Carassius auratus as a bioindicator of the health status of Lake Trasimeno and risk assessment for consumers

Submitted: 31 December 2022
Accepted: 20 March 2023
Published: 18 July 2023
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Fish are good bio-indicators of the health status of the aquatic environment and can be used as biomarkers to assess the aquatic behavior of environmental pollutants, the exposure of aquatic organisms, and the health risk for consumers. Goldfish are a significant bioindicator in the Lake Trasimeno aquatic system (Umbria, Italy). This study aimed to characterize the health status and the chemical and biotic contamination of Lake Trasimeno to define its anthropogenic and natural pressures and the risk associated with consuming its fishery products. 114 determinations were performed on Carassius auratus samples from 2018 to 2020, and the occurrence of brominated flame retardants, non-dioxin-like polychlorinated biphenyls, heavy metals, and microplastics was analytically investigated. Dietary exposure assessment, risk characterization, and benefit-risk evaluation were performed for schoolchildren from 3 to 10 years old. Flame-retardants registered high levels of non-detects (99% for polybrominated diphenyl ether and 76% for hexabromocyclododecanes), while polychlorinated biphenyls were found in all samples with a maximum level of 56.3 ng/g. Traces of at least one heavy metal were found in all samples, though always below the regulatory limit. Microplastics were found with a 75% frequency of fish ingesting at least one particle. Dietary exposure and risk characterization reveal negligible contributions to the reference values of all contaminants, except for mercury, which reached up to 25% of admissible daily intake. The benefit-risk assessment highlighted that the benefits of freshwater fish intake outweigh the associated risks. The examination of goldfish as indicator fish reveals the quality of Lake Trasimeno's aquatic environment and the safety of its products.

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Abdi K, Azadikhah D, Fard AN, 2014. Occurrence reported the Aeromonas sobria infection in goldfish (Carassius auratus). In: Proceedings of the Iranian Veterinary Congress in Teheran, volume 18.
Aliko V, Qirjo M, Sula E, Morina V, Faggio C, 2018. Antioxidant defense system, immune response and erythron profile modulation in gold fish, Carassius auratus, after acute manganese treatment. Fish Shellfish Immunol 76:101-9.
Ašmonaite G, Larsson K, Undeland I, Sturve J, Carney Almroth B, 2018. Size matters: ingestion of relatively large microplastics contaminated with environmental pollutants posed little risk for fish health and fillet quality. Environ Sci Technol 52:14381-91.
Avio CG, Gorbi S, Regoli F, 2015. Experimental development of a new protocol for extraction and characterization of microplastics in fish tissues: first observations in commercial species from Adriatic Sea. Mar Environ Res 111:18-26.
Avio CG, Pittura L, d’Errico G, Abel S, Amorello S, Marino G, Regoli F, 2020. Distribution and characterization of microplastic particles and textile microfibers in Adriatic food webs: general insights for biomonitoring strategies. Environ Pollut 258:113766.
Barchiesi F, Branciari R, Latini M, Roila R, Lediani G, Filippini G, Scortichini G, Piersanti A, Rocchegiani E, Ranucci D, 2020. Heavy metals contamination in shellfish: benefit-risk evaluation in central Italy. Foods 9:1720.
Barghi M, Shin ES, Son MH, Choi SD, Pyo H, Chang YS, 2016. Hexabromocyclododecane (HBCD) in the Korean food basket and estimation of dietary exposure. Environ Pollut 213:268-77.
Benford DJ, 2013. Risk assessment of chemical contaminants and residues in foods. In: Rose M, Fernandez A (eds). Persistent organic pollutants and toxic metals in foods. Cambridge, UK: Woodhead Publishing. pp. 173-87.
Bernet D, Schmidt H, Meier W, Burkhardt‐Holm P, Wahli T, 2001. Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 22:25-34.
Besis A, Christia C, Poma G, Covaci A, Samara C, 2017. Legacy and novel brominated flame retardants in interior car dust - implications for human exposure. Environ Pollut 230:871-81.
Bessa F, Frias J, Kögel T, Lusher A, Andrade J, Antunes JC, Sobral P, Pagter E, Nash R, O'Connor I, Pedrotti ML, Keros E, León VM, Tirelli V, Suaria G, Lopes C, Raimundo J, Caetano M, Gago J, Viñas L, Carretero O, Magnusson K, Granberg M, Dris R, Fischer M, Scholz-Böttcher BM, Lorenzo SM, Grueiro G, Fernández-González V, Palazzo L, Camedda A, de Lucia GA, Avio CG, Gorbi S, Pittura L, Regoli F, Gerdts G, 2019. Harmonized protocol for monitoring microplastics in biota. Deliverable 4.3. Available from: https://www.researchgate.net/publication/332157735_Harmonized_protocol_for_monitoring_microplastics_in_biota.
Bonanomi S, Colombelli A, Bucciarelli B, De Angelis R, Sala A, 2019. Serving local fish in school meals: the nutritional importance of consuming oily fish. Sustainability 11:3990.
Bour A, Avio CG, Gorbi S, Regoli F, Hylland K, 2018. Presence of microplastics in benthic and epibenthic organisms: influence of habitat, feeding mode and trophic level. Environ Pollut 243:1217-25.
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 Pub Health 17:2545.
Branciari R, Roila R, Ranucci D, Altissimi MS, Mercuri ML, Haouet NM, 2020. Estimation of acrylamide exposure in Italian schoolchildren consuming a canteen menu: health concern in three age groups. Int J Food Sci Nutr 71:122-31.
Burgos-Aceves MA, Cohen A, Smith Y, Faggio C, 2018. MicroRNAs and their role on fish oxidative stress during xenobiotic environmental exposures. Ecotoxicol Environ Saf 148:995-1000.
Carosi A, Ghetti L, Lorenzoni M, 2017. Invasive Carassius spp. in the Tiber river basin (Umbria, central Italy): population status and possible interactions with native fish species. Cybium 41:11-23.
Cera A, Sighicelli M, Sodo A, Lecce F, Menegoni P, Scalici M, 2022. Microplastics distribution and possible ingestion by fish in lacustrine waters (Lake Bracciano, Italy). Environ Sci Pollut Res 29:68179-90.
Christensen KY, Raymond M, Blackowicz M, Liu Y, Thompson BA, Anderson HA, Turyk M, 2017. Perfluoroalkyl substances and fish consumption. Environ Res 154:145-51.
Covaci A, Gheorghe A, Hulea O, Schepens P, 2006. Levels and distribution of organochlorine pesticides, polychlorinated biphenyls and polybrominated diphenyl ethers in sediments and biota from the Danube delta, Romania. Environ Pollut 140:136-149.
Domingo JL, 2016. Nutrients and chemical pollutants in fish and shellfish. Balancing health benefits and risks of regular fish consumption. Crit Rev Food Sci Nutr 56:979-88.
EPA, 2009. State of the great lakes 2009. Available from: https://archive.epa.gov/solec/web/pdf/sogl_2009_h_en-1.pdf.
EFSA, 2005. Opinion of the scientific committee on a request from efsa related to a harmonized approach for risk assessment of substances which are both genotoxic and carcinogenic. EFSA J 282:1-31.
EFSA, 2006. Guidance of the scientific committee on a request from EFSA related to uncertainties in dietary exposure assessment. EFSA J. 2006, 438, 1–54.
EFSA, 2010. Management of left-censored data in dietary exposure assessment of chemical substances. EFSA J 8:1557.
EFSA, 2011a. Scientific opinion on polybrominated diphenyl ethers (PBDEs) in food. EFSA J 9:2156.
EFSA, 2011b. Panel on Contaminants in the Food Chain (CONTAM). Statement on tolerable weekly intake for cadmium. Efsa J 2011;9:1975.
EFSA, 2012. Scientific opinion on the tolerable upper intake level of eicosapentaenoic acid (EPA), docosahexaenoic acid (DHA) and docosapentaenoic acid (DPA). EFSA J 10:2815.
EFSA, 2015. Statement on the benefits of fish/seafood consumption compared to the risks of methylmercury in fish/seafood. EFSA J 13:3982.
EFSA, 2018. Scientific opinion on the risk for public health related to the presence of mercury and methylmercury in food. EFSA J 10:2985.
EFSA, 2021. Update of the risk assessment of hexabromocyclododecanes (HBCDDS) in food. EFSA J 19:06421.
European Commission, 2006. Commission regulation (EC) no 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs (text with EEA relevance). In: Official Journal, L 364/5, 20/12/2006.
European Commission, 2007. Commission regulation (EC) no 333/2007 of 28 March 2007 laying down the methods of sampling and analysis for the official control of the levels of lead, cadmium, mercury, inorganic tin, 3-mcpd and benzo(a)pyrene in foodstuffs. In: Official Journal, L 88/29, 29/03/2007.
European Commission, 2017. Commission regulation (EU) 2017/644 of 5 April 2017 laying down methods of sampling and analysis for the control of levels of dioxins, dioxin-like PCBs and non-dioxin-like PCBS in certain foodstuffs and repealing regulation (EU) no 589/2014. In: Official Journal, L 92/9, 6/04/2017.
European Union reference laboratory for halogenated POPs in feed and food. Available online: https://food.ec.europa.eu/horizontal-topics/european-union-reference-laboratories_en. Accessed: 10/03/2022.
FAO/WHO, 2001. Joint FAO/WHO food standards programme, codex committee on food additives and contaminants. In: Proceedings of the 33rd Session CODEX, Hague, The Netherlands, 12-16 March 2001. pp. 121-6.
Fernandes A, Mortimer D, Rose M, Smith F, Panton S, Garcia-Lopez M, 2016. Bromine content and brominated flame retardants in food and animal feed from the UK. Chemosphere 150:472-8.
Fliedner A, Rüdel H, Lohmann N, Buchmeier G, Koschorreck J, 2018. Biota monitoring under the water framework directive: on tissue choice and fish species selection. Environ Pollut 235:129-40.
Geng JJ, Li H, Liu JP, Yang Y, Jin ZL, Zhang YN, Zhang ML, Chen LQ, Du ZY, 2015. Nutrients and contaminants in tissues of five fish species obtained from Shanghai markets: risk-benefit evaluation from human health perspectives. Sci Total Environ 536:933-45.
Ludovisi A, Gaino E, 2010. Meteorological and water quality changes in Lake Trasimeno (Umbria, Italy) during the last fifty years. Journal of Limnology 69:174-88.
Majtán J, Černy J, Ofúkaná A, Takáč P, Kozánek M, 2012. Mortality of therapeutic fish Garra rufa caused by Aeromonas sobria. Asian Pac J Trop Biomed 2:85-7.
Orban E, Nevigato T, Masci M, Di Lena G, Casini I, Caproni R, Gambelli L, De Angelis P, Rampacci M, 2007. Nutritional quality and safety of perch (perca fluviatilis) from three lakes of Central Italy. Food Chem 100:482-90.
Pieniak Z, Verbeke W, Olsen SO, Hansen KB, Brunsø K, 2010. Health-related attitudes as a basis for segmenting European fish consumers. Food Policy 35:448-55.
Piersanti A, Amorena M, Manera M, Tavoloni T, Lestingi C, Perugini M, 2012. PCB concentrations in freshwater wild brown trouts (Salmo trutta trutta l) from Marche rivers, central Italy. Ecotoxicol Environ Saf 84:355-9.
Primpke S, Cross RK, Mintenig SM, Simon M, Vianello A, Gerdts G, Vollertsen J, 2020. Toward the systematic identification of microplastics in the environment: evaluation of a new independent software tool (simple) for spectroscopic analysis. Appl Spectrosc 74:1127-38.
Roila R, Branciari R, Ranucci D, Stramenga A, Tavoloni T, Stecconi T, Piersanti A, 2021. Risk characterization and benefit-risk assessment of brominated flame retardant in commercially exploited freshwater fishes and crayfish of Lake Trasimeno, Italy. Int J Environ Res Public Health 18:8763.
Roila R, Branciari R, Verdini E, Ranucci D, Valiani A, Pelliccia A, Pecorelli I, 2021. A study of the occurrence of aflatoxin M1 in milk supply chain over a seven-year period (2014-2020): human exposure assessment and risk characterization in the population of central Italy. Foods 10:1529.
Shim WJ, Thomposon RC, 2015. Microplastics in the ocean. Arch Environ Contam Toxicol 69:265-8.
Su G, Saunders D, Yu Y, Yu H, Zhang X, Liu H, Giesy JP, 2014. Occurrence of additive brominated flame retardants in aquatic organisms from Tai lake and Yangtze river in eastern China, 2009-2012. Chemosphere 114:340-6.
Tavoloni T, Stramenga A, Stecconi T, Siracusa M, Bacchiocchi S, Piersanti A, 2020. Single sample preparation for brominated flame retardants in fish and shellfish with dual detection: GC-MS/MS (PBDEs) and LC-MS/MS (HBCDS). Anal Bioanal Chem 412:397-411.
Tijhuis M, de Jong N, Pohjola M, Gunnlaugsdóttir H, Hendriksen M, Hoekstra J, Holm F, Kalogeras N, Leino O, van Leeuwen F, Lutejin JM, Magnússon SH, Odekerken G, Rompelberg C, Tuomisto JT, Ueland Ø, White BC, Verhagen H, 2012. State of the art in benefit-risk analysis: food and nutrition. Food Chem Toxicol 50:5-25.
Toussaint B, Raffael B, Angers-Loustau A, Gilliland D, Kestens V, Petrillo M, Rio-Echevarria IM, Van den Eede G, 2019. Review of micro-and nanoplastic contamination in the food chain. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 36:639-73.
USEPA-IRIS, 2008a. 2,20,4,40-tetrabromodiphenyl ether (bde-47) (casrn 5436-43-1 | dtxsid 3030056. Available from: https://cfpub.epa.gov/ncea/iris2/chemicallanding.cfm?substance_nmbr=1010. Accessed: 25 June 2022.
USEPA-IRIS, 2008b. 2,20,4,40,5-pentabromodiphenyl ether (BDE-99) (CASRN 60348-60-9 | DTXSID 9030048). Available from: https://cfpub.epa.gov/ncea/iris2/chemicallanding.cfm?substance_nmbr=1008. Accessed: 25 June 2022.
USEPA-IRIS, 2008c. 2,20,4,40,5,50-hexabromodiphenyl ether (BDE-153) (CASRN 68631-49-2 | DTXSID 4030047). Available from: https://cfpub.epa.gov/ncea/iris2/chemicalLanding.cfm?substance_nmbr=1009. Accessed: 25 June 2022.
USEPA-IRIS, 2008d. 2,20,3,30,4,40,5,50,6,60-decabromodiphenyl ether (BDE-209) (CASRN 1163-19-5 | DTXSID 9020376). Available from: https://iris.epa.gov/ChemicalLanding/&substance_nmbr=35. Accessed: 25 June 2022.
Van der Oost R, Beyer J, Vermeulen NP, 2003. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57-149.
Yang J, Chen L, Liu LZ, Shi WL, Meng XZ, 2014. Comprehensive risk assessment of heavy metals in lake sediment from public parks in Shanghai. Ecotoxicol Environ Saf 102:129-35.
Yi YJ, Zhang SH, 2012. Heavy metal (Cd, Cr, Cu, Hg, Pb, Zn) concentrations in seven fish species in relation to fish size and location along the Yangtze river. Environ Sci Pollut Res 19:3989-96.
Zhang Y, Wu JP, Luo X, Sun Y, Mo L, Chen SJ, Mai BX, 2011. Biota-sediment accumulation factors for dechlorane plus in bottom fish from an electronic waste recycling site, south China. Environ Int 37:1357-61.

How to Cite

1.
Roila R, Piersanti A, Valiani A, Ranucci D, Tavoloni T, Stramenga A, Griffoni F, Pittura L, Gorbi S, Franceschini R, Agnetti F, Palma G, Branciari R. <i>Carassius auratus</i> as a bioindicator of the health status of Lake Trasimeno and risk assessment for consumers. Ital J Food Safety [Internet]. 2023 Jul. 18 [cited 2024 Nov. 23];12(3). Available from: https://www.pagepressjournals.org/ijfs/article/view/11137