Abstract
Flame retardants are compounds added to a high diversity of polymers used in electronics and furniture to decrease the risk of combustion. Decabromodiphenyl ether (BDE-209) is a polybrominated diphenyl ether (PBDE) congener still used worldwide, while 2, 4, 6-tribromophenol(TBP) is a PBDE metabolite used as a pesticide and flame retardant for wood conservation. These compounds have lipophilic properties and are easily bioaccumulated in the food chain. In the current study, the acute and chronic toxicity of BDE-209 and TBP was evaluated in Oreochromis niloticus through analyses of redox imbalance, neurotoxicity, and histopathological biomarkers after acute (24, 48, 72, and 96 h) and chronic (90 days) exposure to 0.5, 5, and 50 ng/g of the polybrominated compounds. The results showed effects on glutathione S-transferase(GST) activity and damage to biomolecules in both acute and chronic exposures. Liver histopathology and the ultrastructure of hepatocytes revealed alterations and damage in individuals from both experiments, but only BDE-209 led to neurotoxic effects. The current study revealed new endpoints related to polybrominated compounds in fish, highlighting the need to review the risk of exposure to biota.
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The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Aznar-Alemany O, Trabalon L, Jacobs S, Barbosa VL, Tejedor MF, Granby K, Kwadijk C, Cunha SC, Ferrari F, Vandermeersch G, Sioen I, Verbeke W, Vilavert L, Domingo JL, Eljarrat E, Barcelo D (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
Barja-Fernández S, Jesús M, Álvarez-Otero MR (2013) Histopathological effects of 2,2′,4,4′-tetrabromodiphenyl ether (BDE-47) in the gills, intestine and liver of turbot (Psetta maxima). Ecotox Environ Safety 95:60–68. https://doi.org/10.1016/j.ecoenv.2013.05.028
Beliaeff B, Burgeot T (2002) Integral biomarker response: a useful tool for ecological risk assessment. Environ Toxicol Chem 21(6):1316–1322. https://doi.org/10.1897/1551-5028(2002)021
Bernet D, Schmidt H, Meier W, Burkhardt-Holm P, Wahli T (1999) Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 22:25–34. https://doi.org/10.1046/j.1365-2761.1999.00134.x
Boelsterli A (2007) Mechanistic toxicology. The molecular basis of how chemicals disrupt biological targets, Second Edition. Published March 23, 2007 by CRC Press. 416 Pages 210 B/W
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 7(72):248–254. https://doi.org/10.1006/abio.1976.9999
Chen MH, Ma WL (2021) A review on the occurrence of organophosphate flame retardants in the aquatic environment in China and implications for risk assessment. Sci Total Environ 147064. https://doi.org/10.1016/j.scitotenv.2021.147064
Chokwe TB, Krȕger E, Magubane MN, Abafe O, Mportji S, Okonkwo OJ, Sibali L, Hariram R (2018) Legacy and novel brominated flame-retardants in different fish types from inland freshwaters of South Africa: levels, distribution and implications for human health. Inter J Environ Health Res. https://doi.org/10.1080/09603123.2020.1757042
Chung HY, Ma WCJ, Kim JS (2003) Seasonal distribution of bromophenols in selected Hong Kong seafood. J Agric Food Chem 51:6752–6760. https://doi.org/10.1021/jf034632r
Clemente D, Porteros A, Weruaga E, Alonso JR, Arenzana FJ, Aijón J et al (2004) Cholinergic elements in the zebrafish central nervous system: histochemical and immunohistochemical analysis. J Comp Neurol 474(1):75–107. https://doi.org/10.1002/cne.20111
Covaci A, Harrad S, Abdallah MAE, Ali N, Law RJ, Herzke D, de Wit CA (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
Deng J, Liu C, Yu L, Zhou B (2010) Chronic exposure to environmental levels of tribromophenol impairs zebrafish reproduction. Toxicol Appl Pharmacol 243(1):87–95. https://doi.org/10.1016/j.taap.2009.11.016
Ellman GL, Courtney KO, Andres V, Featherstone RMA (1961) New and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95. https://doi.org/10.1016/0006-2952(61)90145-9
Folle NMT, Azevedo-linhares M, Garcia JE, Esquivel L, Oliveira EC, Filipak Neto F, Oliveira Ribeiro CA (2021) 2,4,6-Tribromophenol is toxic to Oreochromis niloticus (Linnaeus, 1758) after trophic and subchronic exposure. Chemosphere 268:128785. https://doi.org/10.1016/j.chemosphere.2020.128785
Folle NMT, Azevedo-Linhares M, Garcia JE, Souza ATC, Grötzner SR, Oliveira EC, Paulin AF, Leite NF, Filipak Neto F, Oliveira Ribeiro CA (2020) Low concentration of 2,4,6-tribromophenol (TBP) represents a risk to South American silver catfish Ramdia quelen (Quoy and Gaimard, 1824) population. Ecotoxicol Environ Saf 187:109815. https://doi.org/10.1016/j.ecoenv.2019.109815
Fu J, Guo Y, Wang M, Yang L, Han J, Lee JS, Zhou B (2020) Bioconcentration of 2,4,6-tribromophenol (TBP) and thyroid endocrine disruption in zebrafish larvae. Ecotoxi Environ Safety 206:111207. https://doi.org/10.1016/j.ecoenv.2020.111207
Gemuse SL, Folle NMT, Souza ATC, Azevedo-Linhares M, Filipak Neto F, Ortolani-Machado CF, Garcia JRE, Esquivel L, Silva CP, Campos SX, Martins CC, Oliveira Ribeiro CA (2021) Micropollutants impair the survival of Oreochromis niloticus and threat local species from Iguaçu River, Southern of Brazil. Environ Toxicol Pharmacol 83:103596. https://doi.org/10.1016/j.etap.2021.103596
Ghosh R, Lokman PM, Lamare MD, Metcalf VJ, Burritt DJ, Davison W, Hageman KJ (2013) Changes in physiological responses of an Antarctic fish, the emerald rock cod (Trematomus bernacchii), following exposure to polybrominateddiphenyl ethers (PBDEs). Aquat Toxicol 128(129):91–100. https://doi.org/10.1016/j.aquatox.2012.11.019
Han Z, Li Y, Zhang S, Song N, Xu H, Dang Y, Liu C, Giesy JP, Yua H (2017) Prenatal transfer of decabromodiphenyl ether (BDE-209) results in disruption of the thyroid system and developmental toxicity in zebrafish offspring. Aquat Toxicol 190:46–52. https://doi.org/10.1016/j.aquatox.2017.06.020
He Y, Peng L, Zhang W, Liu C, Yang Q, Zheng S, Bao M, Huang Y, Wu K (2018) Adipose tissue levels of polybrominated diphenyl ethers and breast cancer risk in Chinese women: A case–control study. Environ Res 167:160–168. https://doi.org/10.1016/J.ENVRES.2018.07.009
Ho KL, Murphy MB, Wan Y, Fong BMW, Tam S, Giesy JP, Leung KS, Lam MHW (2012) Synthesis and characterization of bromophenol glucuronide and sulfate conjugates for their direct LC-MS/MS quantification in human urine as potential exposure markers for polybrominated diphenyl ethers. Anal Chem 84:9881–9888. https://doi.org/10.1021/ac302161t
Hoang AQ, Aono D, Watanabe I, Kuwae M, Kunisue T (2021) Contamination levels and temporal trends of legacy and current-use brominated flame retardants in a dated sediment core from Beppu Bay, southwestern Japan. Chemosphere. 266:129180. https://doi.org/10.1016/j.chemosphere.2020.129180
Jiang ZY, Woollard ACS, Wolff SP (1991) Lipid hydroperoxides measurement by oxidation of Fe2+ in the presence of xylenol orange. Comparison with the TBA assay and an iodometric method. Lipids 26:853–856. https://doi.org/10.1007/BF02536169
Jiang ZY, Hunt JV, Wolff SP (1992) Ferrous ion oxidation in the presence of xylenol orange for detection of lipid hydroperoxide in low density lipoprotein. Anal Biochem 202:384–389. https://doi.org/10.1016/0003-2697(92)90122-n
Kaslin J, Nystedt JM, Ostergård M, Peitsaro N, Panula P (2004) The orexin/hypocretin system in zebrafish is connected to the aminergic and cholinergic systems. J Neurosci 24(11):2678–2689. https://doi.org/10.1523/JNEUROSCI.4908-03.2004
Keen JH, Habig WH, Jakoby WB (1976) Mechanism for several activities of the gluthatione S-transferases. J Biol Chem 251:6183–6188
Koch C, Sures B (2018) Environmental concentrations and toxicology of 2,4,6-tribromophenol (TBP). Environ Pollut 233:706–713. https://doi.org/10.1016/j.envpol.2017.10.127
Lee, HJ, Kim, GB (2015). An overview of polybrominated diphenyl ethers (PBDEs) in the marine environment. Ocean Sci J 50 (2): 119-142. https://doi.org/10.1007/s12601-015-0010-8.
Leonetti C, Butt CM, Hoffman K, Hammel SC, Miranda ML, Stapleton HM (2016) Brominated flame retardants in placental tissues: associations with infant sex and thyroid hormone endpoints. Environ Health 15:113. https://doi.org/10.1186/s12940-016-0199-8
Levine RL, Williams JA, Stadtman EP, Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–357. https://doi.org/10.1016/s0076-6879(94)33040-9
Ma Y, Cui K, Zeng F, Wen J, Liu H, Zhu F, Ouyang G, Luan T, Zeng Z (2013)Microwave-assisted extraction combined with gel permeation chromatography and silica gel cleanup followed by gas chromatography-mass spectrometry for the de-termination of organophosphorus flame retardants and plasticizers in biological samples. Anal Chim Acta 786:47–53. https://doi.org/10.1016/j.aca.2013.04.062
Mueller T, Vernier P, Wullimann MF (2004) The adult central nervous cholinergic system of a neurogenetic model animal, the zebrafish Danio rerio. Brain Res 1011(2):156–169. https://doi.org/10.1016/j.brainres.2004.02.073
Ohta S, Okumura T, Nishimura H, Nakao T, Shimizu Y, Ochiai F, Aozasa O, Miyata H (2004) Human level of PBDEs, TBBPA, TBPs, PCDDs/DFs, PXDDs/DFs and PBDDs/DFs in human milk of nursing woman and dairy milk products in Japan. Organohalogen Compd 66:2857–2862. https://doi.org/10.1016/s0045-6535(01)00233-8
Oliveira Ribeiro CA, dos Reis Filho HS, Grötzner SR (2012) Técnicas e métodos para utilização prática em microscopia. Livraria Santos Editora Ltda, Curitiba, BR, Santos, p 442
Oliveira AS, Silva VM, Veloso MCC, Santos GV, De Andrade JB (2009) Bromophenol concentrations in fish from Salvador, BA, Brazil. Ann Acad Bras Cienc 81:165–172
Pan W, Kang Y, Zeng L, Zhang Q, Ming J, Wong MH (2016) Comparison of in vitro digestion model with in vivo relative bioavailability of BDE-209 in indoor dust and combination of in vitrodigestion/Caco-2 cell model to estimate the daily intake of BDE-209 via indoor dust. Environ Pollut 218:497–504. https://doi.org/10.1016/j.envpol.2016.07.029
Qin S, Yang Z, Zhang S et al (2021) Comparison of flame-retardancy property and mechanism between a phosphate ester and a phosphoramine flame-retardants. J Wuhan Univ Technol Mat Sci 36:148–156. https://doi.org/10.1007/s11595-021-2388-8
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge, UK, 558p
Reineke N, Biselli S, Franke S, Francke W, Heinzel N, Hühnerfuss H, Iznaguen H, Kammann U, Theobald N, Vobach M, Wosniok W (2006) Brominated indoles and phenols in marine sediment and water extracts from the North and baltic seas e concentrations and effects. Arch Environ Contam Toxicol 51:186–196. https://doi.org/10.1007/s00244-005-0135-3
Rios JC, Repetto G, Jos A, del Peso A, Salguero M, Camea A, Repetto M (2003) Tribromophenol induces the differentiation of SH-SY5Y human neuroblastoma cells in vitro. Toxicol in Vitro 17: 635–641https://doi.org/10.1016/S0887-2333(03)00110-3
Ross PS, Couillard CM, Ikonomou MG, Johannessen SC, Lebeuf M, Macdonald RW, Tomy GT (2009) Large and growing environmental reservoirs of deca-BDE present an emerging health risk for fish and marine mammals. Mar Pollut Bull 58:7–10. https://doi.org/10.1016/j.marpolbul.2008.09.002
Rubio-Vargas DA, Oliveira Ribeiro CA, Filipak Neto F, Cordeiro AL, Cestari MM, Souza AC, Martins CC, Silva CP, Campos SX, Garcia JRE, Prodocimo MM (2021) Exposure to pollutants present in Iguaçu River Southern Brazil affect the health of Oreochromis niloticus (Linnaeus, 1758): assessment histological, genotoxic and biochemical. Environ Toxicol Pharmacol 87:103682. https://doi.org/10.1016/j.etap.2021.103682
Sanchez W, Burgeot T, Porcher J (2013) A novel “Integrated Biomarker Response” calculation based on reference deviation concept. Environ Sci Pollut Res 20(5):2721–2725. https://doi.org/10.1007/s11356-012-1359-1
Santana MS, Yamamoto FY, Sandrini-Neto L, Filipak Neto F, Ortolani-Machado CF, Oliveira Ribeiro CA, Prodocimo MM (2018) Diffuse sources of contamination in freshwater fish: detecting effects through active biomonitoring and multi-biomarker approaches. Ecotoxicol Environ Saf 149:173–181. https://doi.org/10.1016/j.ecoenv.2017.11.036
Sedlak J, Lindsay RH (1968) Estimation of total protein bound and nonprotein sulfhydryl groups in tissues with Ellman’s reagent. Anal Biochem 25:192–205. https://doi.org/10.1016/0003-2697(68)90092-4
Sjödin A, Päpke O, McGahee E, Focant JF, Jones RS, Pless-Mulloli T, Toms LML, Herrmann T, Müller J, Needham L, Patterson DG Jr (2008) Concentration of polybrominated diphenyl ethers (PBDEs) in household dust from various countries. Chemosphere. 73(1:131–136. https://doi.org/10.1016/j.chemosphere.2007.08.075
Suzuki G, Takigami H, Watanabe M, Takahashi S, Nose K, Asari M, Sakai S (2008) Identification of brominated and chlorinated phenols as potential thyroid-disrupting compounds in indoor dusts. Environ Sci Technol 42(5):1794–1800. https://doi.org/10.1021/es7021895
Tomy GT, Pleskach K, Oswald T, Halldorson T, Helm PA, Macinnis G, Marvin CH (2008) Enantioselective bioaccumulation of hexabromocyclododecane and congener-specific accumulation of brominated diphenyl ethers in an Eastern Canadian Arctic marine food web. Environ Sci Technol 42:3634–3639. https://doi.org/10.1021/es703083z.
Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149. https://doi.org/10.1016/s1382-6689(02)00126-6
Vieira CED, Costa PG, Lunardelli B, Oliveira LF, Cabrera LC, Risso WE, Primel EG, Meletti PC, Fillmann G, Martinez CBR (2016) Multiple biomarker responses in Prochilodus lineatus subjected to short-term in situ exposure to streams from agricultural areas in Southern Brazil. Sci Total Environ 542:44–56. https://doi.org/10.1016/j.scitotenv.2015.10.0710048-9697
Wang J, Shi X, Du Y, Zhou B (2011) Effects of xenoestrogens on the expression of vitellogenin (vtg) and cytochrome P450 aromatase (cyp19a and b) genes in zebrafish (Danio rerio) larvae. J Environ Sci Health A 46:960–967. https://doi.org/10.1080/10934529.2011.586253
Wang S, Wu C, Liu Z, You H (2018) Studies on the interaction of BDE-47 and BDE-209 with acetylcholinesterase (AChE) based on the neurotoxicity through fluorescence, UV–vis spectra, and molecular docking. Toxicol Lett 287:42–48. https://doi.org/10.1016/j.toxlet.2018.01.018
Wu JP, Guan YT, Zhang Y, Luo X, Zhi H, Chen SJ, Mai BX (2010) Trophodynamics of hexabromocyclododecanes and several other non-PBDE brominated flame retardants in a freshwater food web. Environ Sci Technol 44(14):5490–5495. https://doi.org/10.1021/es101300t
Xie Z, Lu G, Oi P (2014) Effects of BDE-209 and its mixtures with BDE-47and BDE-99 on multiple biomarkers in Carassius auratus. Environ Toxicol Pharmacol 38:554–561. https://doi.org/10.1016/j.etap.2014.08.008
Yamamoto FY, Oliveira Ribeiro CA, Schlenk D (2018) Alterations of cytochrome 450 and the occurrence of persistent organic pollutants in tilapia caged in the reservoirs of the Iguaçu River. 2018. Environ Pollut 240:670–682. https://doi.org/10.1016/j.envpol.2018.04.019
Yu L, Han Z, Liu C (2015) A review on the effects of PBDEs on thyroid and reproduction systems in fish. Gen Comp Endocrinol 219:64–73. https://doi.org/10.1016/j.ygcen.2014.12.010
Acknowledgements
The authors thank technicians from the Center for Advanced Fluorescence Technologies at Federal University of Paraná (UFPR) and the Electron Microscopy Center at UFPR for light and TEM images capture, respectively.
Funding
CNPq (National Council for Scientific and Technological Development – Finance Code 428830/2018-8). The funds were used to possible the experiments as travels, stuffs for experiment design, and chemicals for analysis. Brazilian agencies CAPES (Coordination for the Improvement of Higher Education Personnel - Finance Code 001). This agency is responsible for the institutional fellowship to students who develop the project (Dandie A Bozza).
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Ciro Alberto de Oliveira Ribeiro: participated as the director of the study, presenting ideas, formulation of research goals, and creation of models; was responsible for morphological analysis, provided the study materials, reagents, materials, laboratory samples, animals, instrumentation, or other analysis tools; worked in the original draft including the coordination of manuscript with revisions and execution.
Dandie Antunes Bozza: participated in the development or design of methodology; made the formal analysis and conducted a research and investigation process, specifically performing the experiments, critical review, and commentary.
Luíse Esquivel: participated in the development of experiments and worked critically in the review, commentary, or revision of the manuscript.
Elton Celton de Oliveira: participated in the design and interpretations of model application, all statistical procedures, critical review, commentary, or revision of the manuscript.
Francisco Filipak Neto: participated in ideas and formulation of research goals; also conducted the biochemical analysis and worked in the original draft specifically with critical review, commentary, or revision.
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de Oliveira Ribeiro, C.A., Bozza, D.A., Esquivel, L. et al. Comparative effects of oral exposure to 2, 4, 6-tribromophenol and decabromodiphenyl ether in Nile tilapia. Environ Sci Pollut Res 29, 17087–17102 (2022). https://doi.org/10.1007/s11356-021-16779-x
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DOI: https://doi.org/10.1007/s11356-021-16779-x