Abstract
Occurrence of traditional (PBDEs) and novel (HBB, PBEB, DBDPE) brominated flame retardants, as well as the natural compounds of MeO-PBDEs, were studied in a shellfish species (Hexaplex trunculus) sampled from Bizerte Lagoon. PBDE and MeO-PBDE mean concentrations in murex soft tissues were 187 and 264 ng g−1 lw respectively. The alternative flame retardants were not identified. The sum of PBDE and MeO-PBDE levels recorded in murex from the investigated aquatic ecosystem were comparable or a relatively lower than those reported for other organisms from other regions across the world. The amount of PBDE and MeO-PBDE concentrations from the Bizerte Lagoon recorded in murex were comparable or a relatively lower than those recorded from other areas across the world for other species. There is not a danger to the population health with regard to PBDE intakes associated with the consumption of murex in Bizerte city. We believe that this is the first study of the analysis of these pollutants in marine gastropod mollusks from Tunisian aquatic areas.
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Aznar-Alemany Ò, Aminot Y, Vilà-Cano J et al (2018) Halogenated and organophosphorusflame retardants in European aquaculture samples. Sci Total Environ 612:492–500. https://doi.org/10.1016/j.scitotenv.2017.08.199
Aznar-Alemany Ò, Sala B, Plön S et al (2019) Halogenated and organophosphorus flame retardants in cetaceans from the southwestern Indian Ocean. Chemosphere 226:791–799. https://doi.org/10.1016/j.chemosphere.2019.03.165
Aznar-Alemany Ò, Trabalón L, Jacobs S et al (2017) Occurrence of halogenated flame retardants in commercial seafood species available in European markets. Food Chem Toxicol 104:35–47. https://doi.org/10.1016/j.fct.2016.12.034
Barhoumi B, Menach KL, Clérandeau C et al (2014) Assessment of pollution in the Bizerte lagoon (Tunisia) by the combined use of chemical and biochemical markers in mussels, Mytilus galloprovincialis. Mar Pollut Bull 84:379–390. https://doi.org/10.1016/j.marpolbul.2014.05.002
Barón E, Rudolph I, Chiang G et al (2013) Occurrence and behavior of natural and anthropogenic (emerging and historical) halogenated compounds in marine biota from the Coast of Concepcion (Chile). Sci Total Environ 461–462:258–264. https://doi.org/10.1016/j.scitotenv.2013.05.006
Barón E, Eljarrat E, Barceló D (2014a) Gas chromatography/tandem mass spectrometry method for the simultaneous analysis of 19 brominated compounds in environmental and biological samples. Anal Bioanal Chem 406:7667–7676. https://doi.org/10.1007/s00216-014-8196-7
Barón E, Máñez M, Andreu AC et al (2014b) Bioaccumulation and biomagnification of emerging and classical flame retardants in bird eggs of 14 species from Doñana Natural Space and surrounding areas (South-western Spain). Environ Int 68:118–126. https://doi.org/10.1016/j.envint.2014.03.013
Bartrons M, Grimalt JO, de Mendoza G, Catalan J (2012) Pollutant dehalogenation capability may depend on the trophic evolutionary history of the organism: PBDEs in freshwater food webs. PLoS ONE 7:e41829. https://doi.org/10.1371/journal.pone.0041829
Ben Ameur W, Ben Hassine S, Eljarrat E et al (2011) Polybrominated diphenyl ethers and their methoxylated analogs in mullet (Mugil cephalus) and sea bass (Dicentrarchus labrax) from Bizerte Lagoon, Tunisia. Mar Environ Res 72:258–264. https://doi.org/10.1016/j.marenvres.2011.09.009
Ben Ameur W, El Megdiche Y, Eljarrat E et al (2013) Organochlorine and organobromine compounds in a benthic fish (Solea solea) from Bizerte Lagoon (northern Tunisia): implications for human exposure. Ecotoxicol Environ Saf 88:55–64. https://doi.org/10.1016/j.ecoenv.2012.10.021
Bocio A, Llobet JM, Domingo JL et al (2003) Polybrominated diphenyl ethers (PBDEs) in foodstuffs: human exposure through the diet. J Agric Food Chem 51:3191–3195. https://doi.org/10.1021/jf0340916
Bodin N, N’Gom Ka R, Le Loc’h F et al (2011) Are exploited mangrove molluscs exposed to persistent organic pollutant contamination in Senegal, West Africa? Chemosphere 84:318–327. https://doi.org/10.1016/j.chemosphere.2011.04.012
Byun G-H, Moon H-B, Choi J-H et al (2013) Biomagnification of persistent chlorinated and brominated contaminants in food web components of the Yellow Sea. Mar Pollut Bull 73:210–219. https://doi.org/10.1016/j.marpolbul.2013.05.017
Choo G, Kim DH, Kim UJ et al (2018) PBDEs and their structural analogues in marine environments: fate and expected formation mechanisms compared with diverse environments. J Hazard Mater 343:116–124. https://doi.org/10.1016/j.jhazmat.2017.09.026
Covaci A, Harrad S, Abdallah MA-E et al (2011) Novel brominated flame retardants: a review of their analysis, environmental fate and behaviour. Environ Int 37:532–556. https://doi.org/10.1016/j.envint.2010.11.007
Dahlberg A-K, Bignert A, Legradi J et al (2016) Anthropogenic and naturally produced brominated substances in Baltic herring (Clupea harengus membras) from two sites in the Baltic Sea. Chemosphere 144:2408–2414. https://doi.org/10.1016/j.chemosphere.2015.10.134
Darnerud PO, Eriksen GS, Jóhannesson T et al (2001) Polybrominated diphenyl ethers: occurrence, dietary exposure, and toxicology. Environ Health Perspect 109:49–68. https://doi.org/10.1289/ehp.01109s149
Darnerud PO, Atuma S, Aune M et al (2006) Dietary intake estimations of organohalogen contaminants (dioxins, PCB, PBDE and chlorinated pesticides, e.g. DDT) based on Swedish market basket data. Food Chem Toxicol 44:1597–1606. https://doi.org/10.1016/j.fct.2006.03.011
Du X, Chang H, Zhou Y et al (2017) Polybrominated diphenyl ethers and its methoxylated analogues in biota and sediment samples from two freshwater lakes in Yangtze River delta. Environ Earth Sci 76:171. https://doi.org/10.1007/s12665-017-6499-7
Domingo JL, Bocio A, Falcó G, Llobet JM (2006) Exposure to PBDEs and PCDEs associated with the consumption of edible marine species. Environ Sci Technol 40:4394–4399. https://doi.org/10.1021/es060484k
El Megdiche Y, Ameur WB, Bèchir H et al (2017) Anthropogenic (PBDE) and naturally-produced (MeO-PBDE) brominated compound levels in Bizerte Lagoon clams (Ruditapes decussatus): levels and human health risk assessment. Mar Pollut Bull 125:176–185. https://doi.org/10.1016/j.marpolbul.2017.08.005
Ezechiáš M, Covino S, Cajthaml T (2014) Ecotoxicity and biodegradability of new brominated flame retardants: a review. Ecotoxicol Environ Saf 110:153–167. https://doi.org/10.1016/j.ecoenv.2014.08.030
Govaerts A, Verhaert V, Covaci A et al (2018) Distribution and bioaccumulation of POPs and mercury in the Ga-Selati River (South Africa) and the rivers Gudbrandsdalslågen and Rena (Norway). Environ Int 121:1319–1330. https://doi.org/10.1016/j.envint.2018.10.058
Guo J, Wu F, Shen R, Zeng EY (2010) Dietary intake and potential health risk of DDTs and PBDEs via seafood consumption in South China. Ecotoxicol Environ Saf 73:1812–1819. https://doi.org/10.1016/j.ecoenv.2010.08.009
Hassine SB, Ameur WB, Gandoura N, Driss MR (2012) Determination of chlorinated pesticides, polychlorinated biphenyls, and polybrominated diphenyl ethers in human milk from Bizerte (Tunisia) in 2010. Chemosphere 89:369–377. https://doi.org/10.1016/j.chemosphere.2012.05.035
Hu G, Dai J, Xu Z et al (2010) Bioaccumulation behavior of polybrominated diphenyl ethers (PBDEs) in the freshwater food chain of Baiyangdian Lake, North China. Environ Int 36:309–315. https://doi.org/10.1016/j.envint.2010.01.002
Jin J, Liu W, Wang Y, Yan Tang X (2008) Levels and distribution of polybrominated diphenyl ethers in plant, shellfish and sediment samples from Laizhou Bay in China. Chemosphere 71:1043–1050. https://doi.org/10.1016/j.chemosphere.2007.11.041
Kelly BC, Ikonomou MG, Blair JD, Gobas FAPC (2008) Bioaccumulation behaviour of polybrominated diphenyl ethers (PBDEs) in a Canadian Arctic marine food web. Sci Total Environ 401:60–72. https://doi.org/10.1016/j.scitotenv.2008.03.045
Kierkegaard A, Bignert A, Sellström U et al (2004) Polybrominated diphenyl ethers (PBDEs) and their methoxylated derivatives in pike from Swedish waters with emphasis on temporal trends, 1967–2000. Environ Pollut 130:187–198. https://doi.org/10.1016/j.envpol.2003.12.011
Kiviranta H, Ovaskainen M-L, Vartiainen T (2004) Market basket study on dietary intake of PCDD/Fs, PCBs, and PBDEs in Finland. Environ Int 30:923–932. https://doi.org/10.1016/j.envint.2004.03.002
Kobayashi J, Imuta Y, Komorita T et al (2015) Trophic magnification of polychlorinated biphenyls and polybrominated diphenyl ethers in an estuarine food web of the Ariake Sea, Japan. Chemosphere 118:201–206. https://doi.org/10.1016/j.chemosphere.2014.08.066
Grilo TF, Cardoso PG, Pato P et al (2013) Organochlorine accumulation on a highly consumed bivalve (Scrobicularia plana) and its main implications for human health. Sci Total Environ 461–462:188–197. https://doi.org/10.1016/j.scitotenv.2013.04.096
La Guardia MJ, Hale RC, Harvey E et al (2012) In situ accumulation of HBCD, PBDEs, and several alternative flame-retardants in the bivalve (Corbicula fluminea) and gastropod (Elimia proxima). Environ Sci Technol 46:5798–5805. https://doi.org/10.1021/es3004238
La Nutrition en Tunisie - Informations générales [WWW Document] (n.d.) http://www.institutdenutrition.rns.tn/. Accessed 6 Aug 2019
Lafabrie C, Hlaili AS, Leboulanger C et al (2013) Contaminated sediment resus-pension induces shifts in phytoplankton structure and function in aeutrophic Mediterranean lagoon. Knowl Manag Aquat Ecosyst 410(16):5. https://doi.org/10.1051/kmae/2013060
Lee S, Kannan K, Moon H-B (2013) Assessment of exposure to polybrominated diphenyl ethers (PBDEs) via seafood consumption and dust ingestion in Korea. Sci Total Environ 443:24–30. https://doi.org/10.1016/j.scitotenv.2012.10.099
Li X, Dong S, Wang R et al (2019) Novel brominatedflame retardant (NBFR) concentrations and spatial distribu-tions in globalfishmeal. Ecotoxicol Environ Saf 170:306–313. https://doi.org/10.1016/j.ecoenv.2018.11.112
Liu X, Jiao Y, Lin C et al (2014) PBDEs, hydroxylated PBDEs and methoxylated PBDEs in bivalves from Beijing markets. Chemosphere 110:97–103. https://doi.org/10.1016/j.chemosphere.2014.02.019
Liu Y, Liu J, Yu M et al (2018) Hydroxylated and methoxylated polybrominated diphenyl ethers in a marine food web of Chinese Bohai Sea and their human dietary exposure. Environ Pollut 233:604–611. https://doi.org/10.1016/j.envpol.2017.10.105
Martellini T, Diletti G, Scortichini G et al (2016) Occurrence of polybrominated diphenyl ethers (PBDEs) in foodstuffs in Italy and implications for human exposure. Food Chem Toxicol 89:32–38. https://doi.org/10.1016/j.fct.2015.12.026
McGrath TJ, Ball AS, Clarke BO (2017) Critical review of soil contamination by polybrominated diphenyl ethers (PBDEs) and novel brominated flame retardants (NBFRs); concentrations, sources and congener profiles. Environ Pollut 230:741–757. https://doi.org/10.1016/j.envpol.2017.07.009
Mekni S, Barhoumi B, Aznar-Alemany Ò et al (2019) Occurrence of halogenated flame retardants in sediments and sea urchins (Paracentrotus lividus) from a North African Mediterranean coastal lagoon (Bizerte, Tunisia). Sci Total Environ 654:1316–1325. https://doi.org/10.1016/j.scitotenv.2018.11.139
Meng X-Z, Zeng EY, Yu L-P et al (2007) Assessment of human exposure to polybrominated diphenyl ethers in china via fish consumption and inhalation. Environ Sci Technol 41:4882–4887. https://doi.org/10.1021/es0701560
Moon H-B, Kannan K, Lee S-J, Choi M (2007) Polybrominated diphenyl ethers (PBDEs) in sediment and bivalves from Korean coastal waters. Chemosphere 66:243–251. https://doi.org/10.1016/j.chemosphere.2006.05.025
Munschy C, Héas-Moisan K, Tixier C et al (2011) Classic and novel brominated flame retardants (BFRs) in common sole (Solea solea L.) from main nursery zones along the French coasts. Sci Total Environ 409:4618–4627. https://doi.org/10.1016/j.scitotenv.2011.07.021
Munschy C, Olivier N, Veyrand B, Marchand P (2015) Occurrence of legacy and emerging halogenated organic contaminants in marine shellfish along French coasts. Chemosphere 118:329–335. https://doi.org/10.1016/j.chemosphere.2014.09.106
Ni H-G, Ding C, Lu S-Y et al (2012) Food as a main route of adult exposure to PBDEs in Shenzhen, China. Sci Total Environ 437:10–14. https://doi.org/10.1016/j.scitotenv.2012.07.056
Papachlimitzou A, Barber JL, Losada S et al (2012) A review of the analysis of novel brominated flame retardants. J Chromatogr A 1219:15–28. https://doi.org/10.1016/j.chroma.2011.11.029
She Y-Z, Wu J-P, Zhang Y et al (2013) Bioaccumulation of polybrominated diphenyl ethers and several alternative halogenated flame retardants in a small herbivorous food chain. Environ Pollut 174:164–170. https://doi.org/10.1016/j.envpol.2012.11.024
Sioen I, Bilau M, Verdonck F et al (2008) Probabilistic intake assessment of polybrominated diphenyl ethers and omega-3 fatty acids through fish consumption. Mol Nutr Food Res 52:250–257. https://doi.org/10.1002/mnfr.200700109
Staskal DF, Scott LLF, Haws LC et al (2008) Assessment of polybrominated diphenyl ether exposures and health risks associated with consumption of southern mississippi catfish. Environ Sci Technol 42:6755–6761. https://doi.org/10.1021/es800613k
Sudaryanto A, Setiawan IE, Ilyas M et al (2009) Levels of brominated flame retardants in sediments and their bioaccumulation potential inbiota from Jakarta Bay and its surroundings, Indonesia. In: Obayashi Y, Isobe T, Subramanian A, Suzuki S, Tanabe S (eds) Interdisciplinary studies on environmental chemistry—environmental research in Asia. TERRAPUB, Tokyo, pp 125–131
Sun J, Liu J, Liu Y, Jiang G (2013) Hydroxylated and methoxylated polybrominated diphenyl ethers in mollusks from Chinese coastal areas. Chemosphere 92:322–328. https://doi.org/10.1016/j.chemosphere.2013.03.042
Tao L, Zhang Y, Wu JP et al (2019) Biomagnification of PBDEs and alternative brominated flame retardants in a predatory fish: using fatty acid signature as a primer. Environ Int 127:226–232. https://doi.org/10.1016/j.envint.2019.03.036
Törnkvist A, Glynn A, Aune M et al (2011) PCDD/F, PCB, PBDE, HBCD and chlorinated pesticides in a Swedish market basket from 2005—levels and dietary intake estimations. Chemosphere 83:193–199. https://doi.org/10.1016/j.chemosphere.2010.12.042
Trabalón L, Vilavert L, Domingo JL et al (2017) Human exposure to brominated flame retardants through the consumption of fish and shellfish in Tarragona County (Catalonia, Spain). Food Chem Toxicol 104:48–56. https://doi.org/10.1016/j.fct.2016.11.022
van Leeuwen SPJ, de Boer J (2008) Brominated flame retardants in fish and shellfish—levels and contribution of fish consumption to dietary exposure of Dutch citizens to HBCD. Mol Nutr Food Res 52:194–203. https://doi.org/10.1002/mnfr.200700207
Verhaert V, Covaci A, Bouillon S et al (2013) Baseline levels and trophic transfer of persistent organic pollutants in sediments and biota from the Congo River Basin (DR Congo). Environ Int 59:290–302. https://doi.org/10.1016/j.envint.2013.05.015
Vetter W (2006) Marine halogenated natural products of environmental relevance. Rev Environ Contam Toxicol 188:1–57. https://doi.org/10.1007/978-0-387-32964-2_1
Wang HS, Du J, Ho KL et al (2011) Exposure of Hong Kong residents to PBDEs and their structural analogues through market fish consumption. J Hazard Mater 192:374–380. https://doi.org/10.1016/j.jhazmat.2011.05.036
Weijs L, Das K, Neels H et al (2009) Levels and profiles of persistent organic polluants in several tissues of harbor porpoises (Phoconea phoconea) from the Black Sea. Organohalogen Compd 71:432–436
Yin G, Asplund L, Qiu Y et al (2015) Chlorinated and brominated organic pollutants in shellfish from the Yellow Sea and East China Sea. Environ Sci Pollut Res 22:1713–1722. https://doi.org/10.1007/s11356-014-3198-8
Yin G, Zhou Y, Strid A et al (2017) Spatial distribution and bioaccumulation of polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) in snails (Bellamya aeruginosa) and sediments from Taihu Lake area, China. Environ Sci Pollut Res 24:7740–7751. https://doi.org/10.1007/s11356-017-8467-x
Yu Y-X, Huang N-B, Zhang X-Y et al (2011) Polybrominated diphenyl ethers in food and associated human daily intake assessment considering bioaccessibility measured by simulated gastrointestinal digestion. Chemosphere 83:152–160. https://doi.org/10.1016/j.chemosphere.2010.12.049
Zaccaroni A, Andreini R, Franzellitti S et al (2018) Halogenated flame retardants in stranded sperm whales (Physeter macrocephalus) from the Mediterra-nean Sea. Sci Total Environ 635:892–900. https://doi.org/10.1016/j.scitotenv.2018.04.147
Zhang K, Wan Y, An L, Hu J (2010) Trophodynamics of polybrominated diphenyl ethers and methoxylated polybrominated diphenyl ethers in a marine food web. Environ Toxicol Chem 29:2792–2799. https://doi.org/10.1002/etc.334
Zhen X, Tang J, Xie Z et al (2016) Polybrominated diphenyl ethers (PBDEs) and alternative brominated flame retardants (aBFRs) in sediments from four bays of the Yellow Sea, North China. Environ Pollut 213:386–394. https://doi.org/10.1016/j.envpol.2016.02.042
Zhou Y, Chen Q, Du X et al (2016) Occurrence and trophic magnification of polybrominated diphenyl ethers (PBDEs) and their methoxylated derivatives in freshwater fish from Dianshan Lake, Shanghai, China. Environ Pollut 219:932–938. https://doi.org/10.1016/j.envpol.2016.09.043
Acknowledgements
The Spanish Ministry of Science and Innovation (CEMAGUA-CGL2007-64551/HID) and the Tunisian Ministry of Higher Education and Scientific Research supported this study. The authors are thankful to R. Chaler, D. Fangul, and M. Comesaña for their help at the mass spectrometry work.
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Ameur, W.B., Annabi, A., El Megdiche, Y. et al. Legacy and Emerging Brominated Flame Retardants in Bizerte Lagoon Murex (Hexaplex Trunculus): Levels and Human Health Risk Assessment. Arch Environ Contam Toxicol 78, 337–349 (2020). https://doi.org/10.1007/s00244-019-00694-x
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DOI: https://doi.org/10.1007/s00244-019-00694-x