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Tetrodotoxin Levels of Three Pufferfish Species (Lagocephalus Sp.)

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Tetrodotoxin Levels of Three Pufferfish Species (Lagocephalus Sp.) Chemosphere 219 (2019) 95e99 Contents lists available at ScienceDirect Chemosphere journal homepage: www.elsevier.com/locate/chemosphere Tetrodotoxin levels of three pufferfish species (Lagocephalus sp.) caught in the North-Eastern Mediterranean sea * € Ali Rıza Kosker a, , Fatih Ozogul a, Deniz Ayas b, Mustafa Durmus a,Yılmaz Ucar a, c, € Joe M. Regenstein d, Yesim Ozogul a a Faculty of Fisheries, Çukurova University, Adana, Turkey b Faculty of Fisheries, Mersin University, Mersin, Turkey c Faculty of Marine Sciences, Ordu University, Ordu, Turkey d Department of Food Science, Cornell University, Ithaca, NY 14853-7201, USA highlights graphical abstract Pufferfish are harmful species that have spread rapidly in the Mediter- ranean Sea recently. TTX contents in pufferfish were determined by using the Q-TOF LC/ MS. This is the first report on the TTX content of L. suezensis and L. spadiceus in the Mediterranean Sea. Regardless of TTX levels, L. sceleratus and L. suezensis are highly toxic puf- ferfish that is dangerous for public health. article info abstract Article history: Tetrodotoxin (TTX) levels in Lagocephalus sceleratus (Silverstripe blaasop), Lagocephalus spadiceus (Half- Received 5 September 2018 smooth golden pufferfish) and Lagocephalus suezensis (Suez puffer) caught in Mersin Bay in the North- Received in revised form eastern Mediterranean Sea were analysed using Q-TOF LC/MS. Pufferfish were caught using trawl fishing, 30 November 2018 longlining and fishing line from December 2015 to October 2016. The TTX changes in the gonads, livers, Accepted 1 December 2018 intestines, skins and muscle tissues were evaluated according to sex and season. TTX levels for Available online 3 December 2018 L. sceleratus and L. suezensis for all tissues were in the range of 0.69e35.6 mg/g and 0.67e3.09 mg/g, Handling Editor: J. de Boer respectively. The highest TTX levels were observed in the gonads of female L. sceleratus caught in the autumn, and in the skin of L. suezensis caught in the spring but no quantifiable levels of TTX were found Keywords: for L. spadiceus. In conclusion, L. sceleratus and L. suezensis species caught in the North-Eastern Medi- Marine toxins terranean are toxic, and their consumption is unsafe. Lagocephalus sp. © 2018 Elsevier Ltd. All rights reserved. Pufferfish Tetrodotoxin Q-TOF LC/MS * Corresponding author. Faculty of Fisheries, Cukurova University, 01330, Adana, Turkey. € E-mail addresses: [email protected] (A.R. Kosker), [email protected] (F. Ozogul). https://doi.org/10.1016/j.chemosphere.2018.12.010 0045-6535/© 2018 Elsevier Ltd. All rights reserved. 96 A.R. Kosker et al. / Chemosphere 219 (2019) 95e99 1. Introduction tetrodotoxin-ab120054 (Lot: APN14294-1-1) was used. Before the Q-TOF LC/MS determination, the TTX standard was diluted with Pufferfish species have been in the news in many Mediterranean 0.01 M acetic acid (Merck, Damstadt, Germany) and 4 dilutions countries (Ayas and Kos€ ¸ ker, 2018) because of their toxicity and wide (0.05, 0.1, 0.5, and 1 mg/mL TTX) were prepared from the stock distribution. Pufferfish consumption is considered to be risky. Most solution and a standard curve (r2 ¼ 0.9992) prepared. TTX standard pufferfish contain tetrodotoxin (TTX), which is one of the strongest solutions were kept at À20 C until used, a maximum of 4 wk. marine toxins. It is a non-protein, low molecular weight toxin. TTX is soluble in water and acidic environments, and is odourless and 2.2. Fish samples, identification and measurements tasteless. There are no known antidotes or antitoxins. TTX poi- sonings, caused by pufferfish consumption, occur regularly in Asia, Pufferfish samples that were trawled in the Northeastern especially in Japan (Hwang and Noguchi, 2007; Anonymus, 2018). Mediterranean from December 2015 to October 2016 to cover the 4 TTX poisoning affects the human nervous and mobility (muscle) seasons were obtained from a commercial vessel (Fig. 1). They were systems resulting in visible symptoms such as paralysis, muscle transported to the laboratory in ice for a maximum of 4 h. coordination disorders, respiratory distress and nausea (Isbister Size-weight measurements are shown in Table 1. The maximum et al., 2002). weight values for female and male individuals of L. sceleratus, L. Pufferfish from of Mediterranean Sea, may also have high spadiceus and L. suezensis were 3660, 2750, 832, 809, 92.8 and enough levels of TTX to potentially be toxic and even fatal (Bentur 96.6 g, respectively. The maximum lengths were 65.2 cm for both et al., 2008; Eisenman et al., 2008; Chamandi et al., 2009; Kheifets genders of L. sceleratus, and 36.6, 37.6, 20.5 and 21.0 cm, respec- et al., 2012). To date most studies on pufferfish toxicity in the tively, for the males and females of the other two species. Only Mediterranean Sea have focused on Lagocephalus sceleratus sexually mature pufferfish were used. Gender was determined with (Katikou et al., 2009; Rodriguez et al., 2012; Kosker et al., 2016; Acar the help of a microscope. For each season, 10 males and 10 females et al., 2017; Rambla-Alegre et al., 2017). Some species that came from each species were selected. into the Mediterranean Sea through the Suez Canal are economi- fi cally valuable, while some like puffer sh are considered invasive, 2.3. Samples preparation and TTX extraction poisonous species (Zenetos et al., 2012). Pufferfish have a harmful fi effect on commercially important sh species in addition to their Samples were dissected to take some dorsal muscle (cautiously potential toxicity (Streftaris and Zenetos, 2006; Bentur et al., 2008). avoiding the breakage of the gastrointestinal tract), the liver, in- Thus, many Mediterranean countries have taken some precautions testines, gonads, and the whole upper and lateral skin from head to fi against the possible risks from puffer sh (Kosker et al., 2018b). tail. A total of 80 composite samples were analysed for each species fi Authorities in the European Union banned the shing, landing and with two genders and 4 seasonal groups from 5 different tissue sale of all species in the Tetraodontidae family on the assumption parts, each with three replicates. fi fi that all puffer sh contain toxins. Even though all puffer sh are TTX extraction was carried out using the method of Silva et al. fi considered toxic, some puffer sh do not pose a danger to human (2012). For extraction, one g sample from each part was used. health, and are consumed in many countries (Kosker et al., 2015). Three mL of 1% acetic acid was added. Samples were then ho- fi For example, among the puffer sh common in the Mediterranean mogenized using the Ultra Turrax (IKA T25 Digital Ultra Turrax, fi fi Sea, L. spadiceus was the rst invasive puffer sh coming through Staufen, Germany). Afterwards, it was held in an ultrasonic bath the Suez Canal to become established in the Mediterranean (Bandelin Sonorex RK 100, Berlin, Germany) for 10 min. The (Mavruk and Avsar, 2008). This species is consumed in Eastern mixture was held at room temperature (23 C) for 15 min, and then Asian countries like Japan, Thailand etc. but is among the species centrifuged (Hettich Zentrifugen, Universal 32R, Tuttlingen, Ger- banned by both the European Union (EC, 2004) and the Turkish many) at 4500 g for 20 min at 4 C. The supernatant was removed, Ministry of Food, Agriculture and Livestock (Anonymous, 2016). and 3 mL of 1% acetic acid was added to the residue and the However, no reported cases of poisoning associated with extraction procedures were repeated. The supernatants were L. spadiceus were found in the literature. Studies on L. suezensis combined and brought to 7 mL. The final solution was vortex (ZX3, were quite limited. This species spreading to the coasts of Spain VELP, Usmate, Milan, Italy) mixed with the help of a vacuum ~ from the Eastern Mediterranean within a decade (Izquierdo-Munoz manifold device (Supelco, Bellefonte, PA, USA-57030-U). The and Izquierdo-Gomez, 2014). L. sceleratus also spread quickly, but it has had a negative effect on fishing and public health (Streftaris and Zenetos, 2006). L. sceleratus is the best studied Mediterranean pufferfish with respect to the presence of toxin, which has been definitely found in all cases (Katikou et al., 2009; Rodriguez et al., 2012; Kosker et al., 2016; Acar et al., 2017; Rambla-Alegre et al., 2017). There is one study on the TTX levels of T. flavimaculosus (Kosker et al., 2018a). However, no toxin studies were found for L. spadiceus and L. suezensis in the Mediterranean Sea. Therefore, the effects of gender and season on the toxicity of common Medi- terranean pufferfish, L. sceleratus (Silverstripe blaasop), L. spadiceus (Half-smooth golden pufferfish) and L. suezensis (Suez puffer) were analysed for TTX. 2. Materials and methods 2.1. Tetrodotoxin (TTX) standard The TTX standard was bought from Abcam Biochemicals (Cambridge, UK). For the Q-TOF LC/MS toxin analysis, one mg of Fig. 1. Map of the sampling location. A.R. Kosker et al. / Chemosphere 219 (2019) 95e99 97 Table 1 Length and weight of pufferfish samples. Seasons N Female Male Length (cm) Weight (g) Length (cm) Weight (g) Min-Max Mean ± SD Min-Max Mean ± SD Min-Max Mean ± SD Min-Max Mean ± SD L. sceleratus Winter 10 49.5e65.2 57.2 ± 5.12 1284.2e3661.0 2518.8 ± 846.3 47.6e65.2 57.0 ± 6.14 1268.2e2746.8 2052.9 ± 549.1 Spring 10 46.2e64.9 55.6 ± 6.12 1152.4e3131.5 2163.7 ± 734.0 44.9e55.9 50.5 ± 3.75 1074.5e2196.6 1635.0 ± 379.5 Summer 10 45.9e54.1 49.8 ± 3.14 943.1e1729.8 1337.4 ± 289.0 43.3e45.2 44.4 ± 0.83 784.8e996.2 891.0 ± 88.5 Autumn 10 48.1e63.1 55.7 ± 5.24 1120.2e3243.2 2121.9 ± 743.7 44.7e60.6 52.7 ± 5.26 1154.1e2274.1 1713.3 ± 394.6 L.
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