Eustrongylides spp. parasite risk management in Atherina boyeri from Lake Trasimeno
https://doi.org/10.4081/ijfs.2023.11338
Accepted: 11 July 2023
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Atherina boyeri is the primary source of fishing profit in Lake Trasimeno and a common host for Eustrongylides spp. larvae. The presence of Eustrongylides in fish is a public health concern, and effective risk management procedures are necessary to guarantee that infected products do not reach the market. Currently, in the European Union, there is no official sampling plan for fresh fish that defines sample size, inspection methods, and criteria for accepting or rejecting the product. An approach to Eustrongylides risk management is proposed in this study. A total of 270 batches of A. boyeri, each consisting of 29 specimens, were collected and examined visually in 3 years (2020-2023). The prevalence of the parasite was 20% in 2020, and in the first months of 2021, it grew up to ⁓40%, then dropped to 12.50% in December 2021 and settled at 16% in February 2022. In January and February 2023, the prevalence fell below 1%. The mean abundance was calculated and used to establish a threshold value to determine fish marketability. In 2020 and 2021, several batches were judged not marketable, and in some batches, a freezing treatment was implemented to ensure the inactivation of the parasite. In the last months of 2022 and in January and February of 2023, the presence of parasites in captured fish was negligible, and this allowed the marketability of fish as fresh. The proposed sampling plan was effective in preventing the commercialization of potentially hazardous products.
Agnetti F, Sgariglia E, Maresca C, Lo Vaglio G, Serva D, Veronesi F, Ghittino C, Fioravanti ML, 2019. Study on the infection by Eustrongylides sp. (Nematoda: Dioctophymatidae) in lake fish: results of the current research IZSUM03/2015. Sanità Pubblica Veterinaria 114.
Bianco PG, Caputo V, Ferrito V, Lorenzoni M, Nonnis Marzano F, Stefani F, Sabatini A, Tancioni L, 2013. Atherina boyeri Risso, 1810. Available from: http://www.iucn.it/scheda.php?id=1269860072. Accessed: 03/01/2023.
Bjelić-Čabrilo O, Novakov N, Ćirković M, Kostić D, Popović E, Aleksić N, Lujić J, 2013. The first determination of Eustrongylides excisus jägerskiöld, 1909-larvae (Nematoda: Dioctophymatidae) in the pike-perch Sander lucioperca in Vojvodina (Serbia). Helminthologia 50:291-4.
Branciari R, Ranucci D, Miraglia D, Valiani A, Veronesi F, Urbani E, Lo Vaglio G, Pascucci L, Franceschini R, 2016. Occurrence of parasites of the genus Eustrongylides spp. (Nematoda: Dioctophymatidae) in fish caught in Trasimeno Lake, Italy. Ital J Food Saf 5:6130.
Branciari R, Franceschini R, Roila R, Valiani A, Pecorelli I, Piersanti A, Haouet N, Framboas M, Ranucci D, 2020. Nutritional value and contaminant risk assessment of some commercially important fishes and crawfish of Lake Trasimeno, Italy. Int J Environ Res Public Health 17:2545.
Branciari R, Ranucci D, Urbani E, Valiani A, Trabalza-Marinucci M, Dal Bosco A, Franceschini R, 2017. Freshwater fish burgers made from four different fish species as a valuable strategy appreciated by consumers for introducing EPA and DHA into a human diet. J Aquat Food Prod Technol 26:686-94.
Bush AO, Lafferty KD, Lotz M, Shostak AW, 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575-83.
Castiglione D, Di Maggio M, Guardone L, Ricci E, Tinacci L, Guglielmone G, Coltrar M, Susini F, Armani A, 2023. Eustrongylides excisus in fish species caught in the Massaciuccoli Lake (Northwest Tuscany, Italy): implications for freshwater fish quality and public health. Food Control 153:109894.
Centers for Disease Control, 1982. Intestinal perforation caused by larval Eustrongylides - Maryland. MMWR. Morb Mortal Wkly Rep 31:383-4, 389.
Codex Alimentarius Commission, 1969. Codex Alimentarius sampling plans for prepackaged foods. Available from: https://www.academia.edu/34797815/CODEX_SAMPLING_PLANS_FOR_PREPACKAGED_FOODS_AQL_6_5_CODEX_STAN_233_1969. Accessed: 03/01/2023.
Çolak SÖ, 2013. The helminth community of the sand smelt (Atherina boyeri Risso, 1810) from Lake Iznik, Turkey. J Helminthol 87:129-34.
Cole RA, 1999. Eustrongylidosis. In: Friend M, Franson JC (eds). Field manual of wildlife diseases: general field procedures and diseases of birds. Biological Resources Division, Information and Technology Report 1999-2001, U. S. Geological Survey, Washington, DC. pp. 223-8.
Covelli J, 2019. Trovato un parassita nel pesce persico del Ceresio. Available from: https://www.tio.ch/ticino/attualita/1397786/trovato-un-parassita-nel-pesce-persico-del-ceresio. Accessed: 10/01/2023.
Dezfuli BS, Manera M, Lorenzoni M, Pironi F, Shinn AP, Giari L, 2015. Histopathology and the inflammatory response of European perch, Perca fluviatilis muscle infected with Eustrongylides spp. (Nematode). Parasit Vectors 8:227.
Eberhard ML, Hurwitz H, Sun AM, Coletta D, 1989. Intestinal perforation caused by larval Eustrongylides (Nematoda: Dioctophymatoidae) in New Jersey. Am J Trop Med Hyg 40:648-50.
Eberhard ML, Ruiz-Tiben E, Hopkins DR, Farrell C, Toe F, Weiss A, Withers PC, Jenks MH, Thiele EA, Cotton JA, Hance Z, Holroyd N, Cama VA, Tahir MA, Mounda T, 2014. The peculiar epidemiology of Dracunculiasis in Chad. Am J Trop Med Hyg 90:61-70.
European Commission, 2004. Regulation (EC) No 853/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific hygiene rules for the hygiene of foodstuffs. In: Official Journal, L139/55, 30/4/2004; pp. 55-205.
European Commission, 2005. Regulation (EC) No 2074/2005 laying down implementing measures for certain products under Regulation (EC) No 853/2004 of the European Parliament and of the Council and for the organization of official controls under Regulation (EC) No 854/2004 of the European Parliament and of the Council and Regulation (EC) No 882/2004 of the European Parliament and of the Council, derogating from Regulation (EC) No 852/2004 of the European Parliament and of the Council and amending Regulations (EC) No 853/2004 and (EC) No 854/2004. In: Official Journal, L 338, 22/12/2005; pp. 27-42.
EFSA, 2007. Public health risks involved in the human consumption of reptile meat. EFSA J 578:1-55.
Franceschini R, Guardone L, Armani A, Ranucci D, Roila R, Valiani A, Susini F, Branciari R, 2022. Five-years management of an emerging parasite risk (Eustrongylides sp., Nematoda) in a fishery supply chain located on Trasimeno Lake (Italy). Food Control 136:108858.
Freyhof J, Kottelat M, 2008. Atherina boyeri. Available from: www.iucnredlist.org.
Goncharov SL, Soroka NM, Pashkevich IY, Dubovyi AI, Bondar AO, 2018. Infection of predatory fish with larvae of Eustrongylides excisus (Nematoda, Dioctophymatidae) in the delta of the Dnipro river and the Dnipro-buh estuary in Southern Ukraine. Vestnik Zoologii 52:137-44.
Gravina P, Ludovisi A, Moroni B, Vivani R, Selvaggi R, Petroselli C, Cappelletti D, 2022. Geochemical proxies and mineralogical fingerprints of sedimentary processes in a closed shallow lake basin since 1850. Aquat Geochem 28:43-62.
Guardone L, Nucera D, Pergola V, Costanzo F, Costa E, Tinacci L, Guidi A, Armani A, 2017. Visceral larvae as a predictive index of the overall level of fish batch infection in European anchovies (Engraulis encrasicolus): a rapid procedure for food business operators to assess marketability. Int J Food Microbiol 250:12-8.
Guardone L, Ricci E, Susini F, Polsinelli E, Guglielmone G, Armani A, 2021. First detection of Eustrongylides excisus (Nematoda: Dioctophymatidae) in big-scale sand smelt (Atherina boyeri) from the lake Massaciuccoli (Northwest Tuscany, Italy): implications for public health and seafood quality. Food Control 120:107517.
Honcharov SL, Soroka NM, Galat MV, Zhurenko OV, Dubovyi AI, Dzhmil VI, 2022. Eustrongylides (Nematoda: Dioctophymatidae): epizootology and special characteristics of the development biology. Helminthologia 59:127-42.
Liguria region, 1997. Circular Letter n. 1/97.
Lõhmus M, Björklund M, 2015. Climate change: what will it do to fish-parasite interactions? Biol J Linn Soc 116:397-411.
Lombardy region, 1994. Circular Letter VS8/C790/94.
Lorenzoni M, Ghetti L, 2012. Evoluzione della fauna ittica e problematiche gestionali del lago Trasimeno. In: Martinelli (ed.). Tutela ambientale del Lago Trasimeno. Perugia, Italy: Arpa Umbria; pp. 131-45. [Book in Italian].
Lorenzoni M, Giannetto D, Carosi A, Dolciami R, Ghetti L, Pompei L, 2015. Age, growth and body condition of big-scale sand smelt Atherina boyeri Risso, 1810 inhabiting a freshwater environment: Lake Trasimeno (Italy). Knowl Manag Aquat Ecosyst 416:09.
Mazzone A, Caffara M, Gustinelli A, Agnetti F, Sgariglia E, Lo Vaglio G, Fioravanti ML, 2019. Morphological and molecular characterization of larval and adult stages of Eustrongylides excisus (Nematoda: Dioctophymatoidea) with histopathological observations. J Parasitol 105:882-9.
Measures LN, 1988. The development of Eustrongylides tubifex (Nematoda: Dioctophymatoidea) in oligochaetes. J Parasitol 74:294-304.
Menconi V, Riina MV, Pastorino P, Mugetti D, Canola S, Pizzul E, Bona MC, Dondo A, Acutis PG, Prearo M, 2020. First occurrence of Eustrongylides spp. (Nematoda: Dioctophymatidae) in a subalpine lake in Northwest Italy: new data on distribution and host range. Int J Environ Res Public Health 17:4171.
Menconi V, Tedesco P, Pastorino P, Confortini I, Esposito G, Tomasoni M, Mugetti D, Gustinelli A, Dondo A, Pizzul E, Fioravanti ML, Prearo M, 2021. Could fish feeding behaviour and size explain prevalence differences of the Nematode Eustrongylides excisus among species? The case study of Lake Garda. Water 13:3581.
Morey GAM, Tuesta Rojas CA, Rengifo Marin GA, Chuquipiondo Guardia CT, 2022. Occurrence of Eustrongylides sp. (Nematoda: Dioctophymatidae) in fish species collected in the Peruvian Amazonia and its implications for public health. Acta Parasitol 67:1432-9.
Narr LL, O’Donnell JG, Libster B, Alessi P, Abraham D, 1996. Eustrongylidiasis - a parasitic infection acquired by eating live minnows. J Osteopathic Med 96:400-2.
Parco Valle Lambro, 2019. Presenza parassiti nel pesce del lago Montorfano. Available from: https://www.parcovallelambro.it/news/presenza-parassiti-nel-pesce-del-lago-montorfano. Accessed: 03/01/2023.
Pietrock M, Marcogliese DJ, 2003. Free-living endohelminth stages: at the mercy of environmental conditions. Trends Parasitol 19:293-9.
Quignard JP, Pras A, 1986. Atherinidae. In: Whitehead P, Bauchot ML, Hureau JC, Nielsen J, Tortonese E (eds.). Fishes of the North-eastern Atlantic and Mediterranean. Paris, France: UNESCO; pp. 1207-10.
Robertson LJ, 2018. Parasites in food: from a neglected position to an emerging issue. Adv Food Nutr Res 86:71-113.
Rusconi A, Prati P, Bragoni R, Castelli M, Postiglione U, Rigamonti S, Sassera D, Olivieri E, 2022. Occurrence of Eustrongylides excisus (Nematoda: Dioctophymatidae) in European perch (Perca fluviatilis) and great cormorant (Phalacrocorax carbo) in Lake Annone, Northern Italy. J Parasitol 108:209-16.
Shamsi S, Sheorey H, 2018. Seafood‐borne parasitic diseases in Australia: are they rare or underdiagnosed? Intern Med J 48:591-6.
Spalding MG, Forrester DJ, 2008. Eustrongylidosis. In: Atkinson CT, Thomas NJ, Hunter DB (eds.). Parasitic diseases of wild birds. Ames, Iowa, USA: John Wiley & Sons, Inc-Blackwell Publishing; pp. 289-315.
Spalding MG, Forrester DJ, 1993. Pathogenesis of Eustrongylides ignotus (Nematoda: Dioctophymatoidea) in Ciconiiformes. J Wildl Dis 29:250-60.
Whitehead PJP, Bauchot ML, Hureau JC, Nielsen J, Tortonese E, 1986. Fishes of the Northeastern Atlantic and the Mediterranean. Paris, France: UNESCO.
Wittner M, Turner JW, Jacquette G, Ash LR, Salgo MP, Tanowitz HB, 1989. Eustrongylidiasis - a parasitic infection acquired by eating sushi. N Engl J Med 320:1124-6.
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