https://doi.org/10.4081/ijfs.2023.11117
Accidental discovery of a Tetraodontidae (Sphoeroides marmoratus) within a cuttlefish (Sepia officinalis) bought in a fish shop in Italy: risk assessment associated with the presence of Tetrodotoxin
Submitted: 27 December 2022
Accepted: 14 February 2023
Published: 8 June 2023
Accepted: 14 February 2023
Abstract Views: 1477
PDF: 275
HTML: 6
HTML: 6
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
Authors
The discovery of a pufferfish specimen (Tetraodontidae) inside a frozen cuttlefish, purchased by a fishmonger, and caught in the central-east Atlantic (FAO 34) is reported. The consumer, who reported this case to FishLab (Department of Veterinary Sciences, University of Pisa) for investigation, was a student of Veterinary Medicine at the University of Pisa. He recognized the Tetraodontidae because he attended practical lessons on fish morphological identification during the course of food inspection and was aware of the risks to human health linked to the Tetrodotoxin (TTX). In this study, the pufferfish was identified morphologically, using the FAO morphological keys, and molecularly, analyzing two markers, the cytochrome oxidase I (COI) and the cytochrome b genes, by DNA barcoding. The pufferfish was identified morphologically as Sphoeroides spp., and molecularly as Sphoeroides marmoratus using the COI gene (99-100% identity values). Literature reports that S. marmoratus from the eastern Atlantic contains high concentrations of TTX in the gonads and the digestive tract. However, the possible passage of TTX from fish to other organisms linked to contact or ingestion has never been reported. This represents the first case of a potentially toxic pufferfish entering the market inside another organism. The fact that a student observed this occurrence highlights the key role of citizen science in the management of emerging risks.
Armani A, Guardone L, La Castellana R, Gianfaldoni D, Guidi A, Castigliego L, 2015. DNA barcoding reveals commercial and health issues in ethnic seafood sold on the Italian market. Food Control 55:206-14.
DOI: https://doi.org/10.1016/j.foodcont.2015.02.030
Bane V, Lehane M, Dikshit M, O’Riordan A, Furey A, 2014. Tetrodotoxin: chemistry, toxicity, source, distribution and detection. Toxins 6:693-755.
DOI: https://doi.org/10.3390/toxins6020693
Colapisci, 2022. Available from: https://www.colapisci.it/PescItalia/pisces/Tetraodontiformi/Tetradontidi/pescepallaguinea.htm
Den Broeder L, Devilee J, Van Oers H, Schuit AJ, Wagemakers A, 2018. Citizen science for public health. Health Promot Int 33:505-14.
Denac H, Mevissen M, Scholtysik G, 2000. Structure, function and pharmacology of voltage-gated sodium channels. Naunyn Schmiedeb Arch Pharmacol 362:453-79.
DOI: https://doi.org/10.1007/s002100000319
Directorate-general for maritime affairs and fisheries, 2022. Dealing with a wicked guest, with some EU help. Available from: https://oceans-and-fisheries.ec.europa.eu/news/dealing-wicked-guest-some-eu-help-2022-06-02_en.
EFSA, 2017. Risks for public health related to the presence of tetrodotoxin (TTX) and TTX analogues in marine bivalves and gastropods. EFSA J 15:4752-816.
DOI: https://doi.org/10.2903/j.efsa.2017.4752
European Commission, 2004. Regulation of the European Parliament and of the Council of 29 April 2004 laying down specific hygiene rules for on the hygiene of foodstuffs, 853/2004/CE. In: Official Journal, L 139/55, 30/04/2004.
FishBase, 2022. Available from: https://www.fishbase.se/summary/Sphoeroides-marmoratus.html.
Guardone L, Gasperetti L, Maneschi A, Ricci E, Susini F, Guidi A, Armani A, 2018. Toxic invasive pufferfish (Tetraodontidae family) along Italian coasts: assessment of an emerging public health risk. Food Control 91:330-8.
DOI: https://doi.org/10.1016/j.foodcont.2018.04.005
Guardone L, Maneschi A, Meucci V, Gasperetti L, Nucera D, Armani A, 2020. A global retrospective study on human cases of tetrodotoxin (TTX) poisoning after seafood consumption. Food Rev Int 36:645-67.
DOI: https://doi.org/10.1080/87559129.2019.1669162
Giusti A, Guarducci M, Stern N, Davidovich N, Golani D, Armani A, 2019. The importance of distinguishing pufferfish species (Lagocephalus spp.) in the Mediterranean Sea for ensuring public health: evaluation of the genetic databases reliability in supporting species identification. Fish Res 210:14-21.
DOI: https://doi.org/10.1016/j.fishres.2018.10.003
Hall TA, 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95-8.
Hanifin CT, 2010. The chemical and evolutionary ecology of tetrodotoxin (TTX) toxicity in terrestrial vertebrates. Mar Drugs 8:577-93.
DOI: https://doi.org/10.3390/md8030577
Ikeda K, Murakami Y, Emoto Y, Ngy L, Taniyama S, Yagi M, Takatani T, Arakawa O, 2009. Transfer profile of intramuscularly administered tetrodotoxin to non-toxic cultured specimens of the pufferfish Takifugu rubripes. Toxicon 53:99-103.
DOI: https://doi.org/10.1016/j.toxicon.2008.10.018
Isbister GK, Kiernan MC, 2005. Neurotoxic marine poisoning. Lancet Neurol 4:219-28.
DOI: https://doi.org/10.1016/S1474-4422(05)70041-7
ISPRA, 2016. Attenzione al pesce palla maculato è tossico e non va mangiato! Available from: https://www.isprambiente.gov.it/files/comunicati-stampa/2015/Locandina_pesce_palla.pdf.
IZSLT, 2014. 08/14 RC. Cambiamenti climatici e sicurezza alimentare: indagine molecolare, microbiologica e tossicologica sulle specie ittiche tossiche presenti in alcune zone del Mar Tirreno. Istituto Zooprofilattico Lazio e Toscana.
Kono M, Matsui T, Furukawa K, Yotsu-Yamashita M, Yamamori K 2008. Accumulation of tetrodotoxin and 4,9-anhydrotetrodotoxin in cultured juvenile kusafugu Fugu niphobles by dietary administration of natural toxic komonfugu Fugu poecilonotus liver. Toxicon 51:1269-73.
DOI: https://doi.org/10.1016/j.toxicon.2008.02.017
Kosker AR, Özogul F, Ayas D, Durmus M, Ucar Y, Regenstein JM, Özogul Y, 2019. Tetrodotoxin levels of three pufferfish species (Lagocephalus sp.) caught in the North-Eastern Mediterranean sea. Chemosphere 219:95-9.
DOI: https://doi.org/10.1016/j.chemosphere.2018.12.010
Noguchi T, Arakawa O, 2008. Tetrodotoxin - distribution and accumulation in aquatic organisms, and cases of human intoxication. Mar Drugs 6:220-42.
DOI: https://doi.org/10.3390/md20080011
OED, 2022. Available from: https://www.oed.com.
Pinto EP, Rodrigues SM, Gouveia N, Timóteo V, Costa PR, 2019. Tetrodotoxin and saxitoxin in two native species of puffer fish, Sphoeroides marmoratus and Lagocephalus lagocephalus, from NE Atlantic ocean (Madeira Island, Portugal). Mar Environ Res 151:104780.
DOI: https://doi.org/10.1016/j.marenvres.2019.104780
Rambla-Alegre M, Reverté L, del Río V, de la Iglesia P, Palacios O, Flores C, Caixach J, Campbell K, Elliott CT, Izquierdo-Muñoz A, Campàs M, Diogène J, 2017. Evaluation of tetrodotoxins in puffer fish caught along the Mediterranean coast of Spain. Toxin profile of Lagocephalus sceleratus. Environ Res 158:1-6.
DOI: https://doi.org/10.1016/j.envres.2017.05.031
SealifeBase, 2022. Available from: https://www.sealifebase.ca/summary/Sepia-officinalis.html.
Silva M, Rodríguez I, Barreiro A, Kaufmann M, Neto A I, Hassouani M, Sabour B, Alfonso A, Botana LM, Vasconcelos V, 2019. Tetrodotoxins occurrence in non-traditional vectors of the north atlantic waters (Portuguese maritime territory, and morocco coast). Toxins 11:306.
DOI: https://doi.org/10.3390/toxins11060306
Suehiro M, 1994. Historical review on chemical and medical studies of globefish toxin before World War II. Yakushigaku Zasshi 29:428-34.
Tinacci L, Guidi A, Toto A, Guardone L, Giusti A, D’Amico P, Armani A, 2018. DNA barcoding for the verification of supplier’s compliance in the seafood chain: how the lab can support companies in ensuring traceability. Ital J Food Saf 7:6894.
DOI: https://doi.org/10.4081/ijfs.2018.6894
Tonon LAC, de Azevedo GPR, Monteiro A F, Bernardi DI, Gubiani JR, Ióca LP, Mattsson HK, Moreira APB, Gomes AF, Pires Junior OR, Pedrosa CSG, Souza LRQ, Rehen S, Thompson CC, Thompson FL, Berlinck RGS, 2020. New tetrodotoxin analogs in Brazilian pufferfishes tissues and microbiome. Chemosphere 242:1-11.
DOI: https://doi.org/10.1016/j.chemosphere.2019.125211
Vacchi M, Bussotti S, Miglietta AM, Guidetti P, 2007. Presence of the Guinean puffer Sphoeroides marmoratus (Lowe, 1838) in the Mediterranean Sea. J Fish Biol 71:1215-9.
DOI: https://doi.org/10.1111/j.1095-8649.2007.01578.x
Vohland K, Land-Zandstra A, Ceccaroni L, Lemmens R, Perellò J, Ponti M, Samson R, Waghenknecht K, 2021. The science of citizen science evolves. In: Vohland K, Land-Zandstra A, Ceccaroni L, Lemmens R, Perellò J, Ponti M, Samson R, Waghenknecht K (eds). The science of citizen science. Swizterland: Springer Nature Switzerland AG. pp. 1-12. Available from: https://pure.iiasa.ac.at/id/eprint/16993/1/2021_Book_TheScienceOfCitizenScience.pdf.
DOI: https://doi.org/10.1007/978-3-030-58278-4_1
How to Cite
1.
Malloggi C, Tinacci L, Giusti A, Galli F, Dall’Ara S, Marconi P, Gasperetti L, Armani A. Accidental discovery of a Tetraodontidae (<i>Sphoeroides marmoratus</i>) within a cuttlefish (<i>Sepia officinalis</i>) bought in a fish shop in Italy: risk assessment associated with the presence of Tetrodotoxin. Ital J Food Safety [Internet]. 2023 Jun. 8 [cited 2024 Dec. 22];12(2). Available from: https://www.pagepressjournals.org/ijfs/article/view/11117
Copyright (c) 2023 the Author(s)
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
PAGEPress has chosen to apply the Creative Commons Attribution NonCommercial 4.0 International License (CC BY-NC 4.0) to all manuscripts to be published.