Bioaccumulation patterns, trophic transfer characteristics and dietary exposure potential of tetrabromobisphenol A analogs in a coral reef food web of the Xisha Islands, South China Sea

Abstract

As a typical class of novel organic pollutants, tetrabromobisphenol A (TBBPA) analogs have been widely detected in various environmental matrices. Several toxicological studies have highlighted that the accumulation of pollutants is the basis for assessing their ecological effects and potential risks. However, the bioaccumulation and trophic transfer of TBBPA analogs in marine food webs are not fully understood. This study selected the most important coral reef islands in the South China Sea as the study area to investigate the bioaccumulation patterns and trophic transfer characteristics of TBBPA analogs within the tropical marine food web. TBBPA, tetrabromobisphenol S (TBBPS), TBBPA bis(2-hydroxyethyl ether) (TBBPA-BHEE), and TBBPA bis(glycidyl ether) (TBBPA-BGE) are prevalent in water, sediment, and organisms around the Xisha Islands. The concentrations of these compounds varied significantly among species (P < 0.05), with notably higher concentrations of ∑TBBPA analogs observed in invertebrates than in fish. Moreover, the Log BAFs of TBBPA, TBBPS, and TBBPA-BHEE were all lower than 3.30, whereas TBBPA-BGE exhibited high bioaccumulation potential in some species. The concentrations of TBBPA, TBBPS, TBBPA-BHEE, and TBBPA-BGE in organisms were significantly negatively correlated with trophic level (P < 0.05), indicating pronounced trophic dilution effects throughout the food web. In addition, hydrophobicity and metabolism were found to be important factors affecting the bioaccumulation of TBBPA analogs. The results revealed that dietary exposure to seafood poses no significant health risks to the local population.

Keywords

Tetrabromobisphenol A analogs / bioaccumulation / trophic transfer / aquatic food web / dietary exposure

References

[1] Cruz R,Casal S.Brominated flame retardants and seafood safety: a review.Environ Int2015;77:116-31

[2] Sun CS,Hou R.First insights into the bioaccumulation, biotransformation and trophic transfer of typical tetrabromobisphenol A (TBBPA) analogues along a simulated aquatic food chain.J Hazard Mater2024;465:133390

[3] Hou R,Li H.Occurrence, bioaccumulation, fate, and risk assessment of novel brominated flame retardants (NBFRs) in aquatic environments - a critical review.Water Res2021;198:117168

[4] Alaee M,Sjödin A.An overview of commercially used brominated flame retardants, their applications, their use patterns in different countries/regions and possible modes of release.Environ Int2003;29:683-9

[5] Law RJ,de Boer J.Levels and trends of brominated flame retardants in the European environment.Chemosphere2006;64:187-208

[6] Yu G,Cao Z.Brominated flame retardants (BFRs): a review on environmental contamination in China.Chemosphere2016;150:479-90

[7] Xu X,Huang H,Shi T.Distribution, transformation, and toxic effects of the flame retardant tetrabromobisphenol S and its derivatives in the environment: a review.Sci Total Environ2024;948:174799

[8] Covaci A,Abdallah MA,Harrad S.Analytical and environmental aspects of the flame retardant tetrabromobisphenol-A and its derivatives.J Chromatogr A2009;1216:346-63

[9] Altwaiq AM,van Eldik R.Extraction of brominated flame retardants from polymeric waste material using different solvents and supercritical carbon dioxide.Anal Chim Acta2003;491:111-23

[10] de la Torre, A.; Barbas, B.; Sanz, P.; Navarro, I.; Artíñano, B.; Martínez, M. A. Traditional and novel halogenated flame retardants in urban ambient air: gas-particle partitioning, size distribution and health implications.Sci Total Environ2018;630:154-63

[11] Liu LY,Venier M.Trends in the levels of halogenated flame retardants in the Great Lakes atmosphere over the period 2005-2013.Environ Int2016;92-3:442-9

[12] Ali N,Goosey E,Covaci A.“Novel” brominated flame retardants in Belgian and UK indoor dust: implications for human exposure.Chemosphere2011;83:1360-5

[13] Cristale J,Gómez-Canela C.Occurrence and sources of brominated and organophosphorus flame retardants in dust from different indoor environments in Barcelona, Spain.Environ Res2016;149:66-76

[14] Ricklund N,McLachlan MS.An international survey of decabromodiphenyl ethane (deBDethane) and decabromodiphenyl ether (decaBDE) in sewage sludge samples.Chemosphere2008;73:1799-804

[15] Venkatesan AK.Brominated flame retardants in U.S. biosolids from the EPA national sewage sludge survey and chemical persistence in outdoor soil mesocosms.Water Res2014;55:133-42 PMCID:PMC4013270

[16] Meironyté D,Bergman A.Analysis of polybrominated diphenyl ethers in Swedish human milk. A time-related trend study, 1972-1997.J Toxicol Environ Health A1999;58:329-41

[17] Covaci A,Abdallah MA.Novel brominated flame retardants: a review of their analysis, environmental fate and behaviour.Environ Int2011;37:532-56

[18] Darnerud PO,Jóhannesson T,Viluksela M.Polybrominated diphenyl ethers: occurrence, dietary exposure, and toxicology.Environ Health Perspect2001;109 Suppl 1:49-68 PMCID:PMC1240542

[19] Law K,Danell R.Bioaccumulation and trophic transfer of some brominated flame retardants in a Lake Winnipeg (Canada) food web.Environ Toxicol Chem2006;25:2177-86

[20] Sjödin A,Bergman A.A review on human exposure to brominated flame retardants - particularly polybrominated diphenyl ethers.Environ Int2003;29:829-39

[21] Ding Y,Feng W.Tetrabromobisphenol S alters the circadian rhythm network in the early life stages of zebrafish.Sci Total Environ2022;806:150543

[22] Liu W,Yang L.Developmental toxicity of TCBPA on the nervous and cardiovascular systems of zebrafish (Danio rerio): a combination of transcriptomic and metabolomics.J Environ Sci2023;127:197-209

[23] Jia X,Lin H.TBBPA and its alternative TCBPA induced ROS-dependent mitochondria-mediated apoptosis in the liver of Rana nigromaculata.Environ Pollut2022;297:118791

[24] Kitamura S,Iida M.Anti-thyroid hormonal activity of tetrabromobisphenol A, a flame retardant, and related compounds: affinity to the mammalian thyroid hormone receptor, and effect on tadpole metamorphosis.Life Sci2005;76:1589-601

[25] Ren XM,Xue Q.Binding and activity of tetrabromobisphenol A mono-ether structural analogs to thyroid hormone transport proteins and receptors.Environ Health Perspect2020;128:107008 PMCID:PMC7584160

[26] Roh JY,Kwon JH.Internal concentration and time are important modifiers of toxicity: the case of chlorpyrifos on caenorhabditis elegans.Environ Sci Technol2016;50:9689-96

[27] Fu J,Chen Y.Long-range transport, trophic transfer, and ecological risks of organophosphate esters in remote areas.Environ Sci Technol2021;55:10192-209

[28] Zhang X,Wu Q.Bioaccumulation, trophic transfer, and biotransformation of polychlorinated diphenyl ethers in a simulated aquatic food chain.Environ Sci Technol2023;57:5751-60

[29] van der Oost, R.; Beyer, J.; Vermeulen, N. P. Fish bioaccumulation and biomarkers in environmental risk assessment: a review.Environ Toxicol Pharmacol2003;13:57-149

[30] Gobas FA,Mackay D.Dynamics of dietary bioaccumulation and faecal elimination of hydrophobic organic chemicals in fish.Chemosphere1988;17:943-62

[31] Bruggeman WA,Wijbenga A.Bioaccumulation of super‐lipophilic chemicals in fish.Toxicol Environ Chem1984;7:173-89

[32] Hakk H.Metabolism in the toxicokinetics and fate of brominated flame retardants - a review.Environ Int2003;29:801-28

[33] Li H,Sun Y.Tetrabromobisphenol A and hexabromocyclododecanes in sediments and biota from two typical mangrove wetlands of South China: distribution, bioaccumulation and biomagnification.Sci Total Environ2021;750:141695

[34] Morris S,Zegers BN.Distribution and fate of HBCD and TBBPA brominated flame retardants in North Sea estuaries and aquatic food webs.Environ Sci Technol2004;38:5497-504

[35] Choo G,Oh JE.Species and habitat-dependent accumulation and biomagnification of brominated flame retardants and PBDE metabolites.J Hazard Mater2019;371:175-82

[36] Han F,Hu F.Solid-phase extraction of seventeen alternative flame retardants in water as determined by ultra-high-performance liquid chromatography-tandem mass spectrometry.J Chromatogr A2019;1602:64-73

[37] Xu W,Cai Z.Analytical chemistry of the persistent organic pollutants identified in the Stockholm Convention: a review.Anal Chim Acta2013;790:1-13

[38] Hou R,Pan Y.Novel brominated flame retardants (NBFRs) in a tropical marine food web from the South China Sea: the influence of hydrophobicity and biotransformation on structure-related trophodynamics.Environ Sci Technol2022;56:3147-58

[39] Zheng G,Shi S.Trophodynamics of emerging brominated flame retardants in the aquatic food web of Lake Taihu: relationship with organism metabolism across trophic levels.Environ Sci Technol2018;52:4632-40

[40] Xie Z,Liu J.Occurrence, bioaccumulation, and trophic magnification of pharmaceutically active compounds in Taihu Lake, China.Chemosphere2015;138:140-7

[41] Chen X,Yang J.High-resolution mass spectrometry-based screening and dietary intake assessment of organophosphate esters in foodstuffs from South China.Sci Total Environ2023;905:167169

[42] Wang H,Gong Y,Zhang T.Occurrence and potential health risks assessment of polycyclic aromatic hydrocarbons (PAHs) in different tissues of bivalves from Hainan Island, China.Food Chem Toxicol2020;136:111108

[43] Boecklen WJ,Cook BA.On the use of stable isotopes in trophic ecology.Annu Rev Ecol Evol Syst2011;42:411-40

[44] Post DM.Using stable isotopes to estimate trophic position: models, methods, and assumptions.Ecology2002;83:703-18

[45] Caquet T.Use of carbon and nitrogen stable isotope ratios to assess the effects of environmental contaminants on aquatic food webs.Environ Pollut2006;141:54-9

[46] Cherel Y,Richard P.Isotopic niches and trophic levels of myctophid fishes and their predators in the Southern Ocean.Limnol Oceanogr2010;55:324-32

[47] Sherwood GD.Stable isotope analysis of some representative fish and invertebrates of the Newfoundland and Labrador continental shelf food web.Estuar Coast Shelf S2005;63:537-49

[48] Du D,Zhou Y.Bioaccumulation, trophic transfer and biomagnification of perfluoroalkyl acids (PFAAs) in the marine food web of the South China Sea.J Hazard Mater2021;405:124681

[49] Ding Y,Wu Z.Bioaccumulation and trophic transfer of organophosphate esters in tropical marine food web, South China Sea.Environ Int2020;143:105919

[50] Wu NN,Xu R.New insight into the bioaccumulation and trophic transfer of free and conjugated antibiotics in an estuarine food web based on multimedia fate and model simulation.J Hazard Mater2024;465:133088

[51] Bannon RO.Using stable isotopes to monitor anthropogenic nitrogen inputs to estuaries.Ecol Appl2008;18:22-30

[52] Peterson GS,Yurista PM.Stable nitrogen isotopes of plankton and benthos reflect a landscape-level influence on great lakes coastal ecosystems.J Great Lakes Res2007;33:27-41

[53] Zhao J,Wang T,Song X.Composition and long-term variation characteristics of coral reef fish species in Yongle Atoll, Xisha Islands, China.Biology2023;12:1062 PMCID:PMC10451685

[54] Li Y,Zou S.Pollution status and trophic transfer of polycyclic aromatic hydrocarbons in coral reef ecosystems of the South China Sea.ICES J Mar Sci2021;78:2053-64

[55] Liu AF,Yu M,Shi JB.Tetrabromobisphenol-A/S and nine novel analogs in biological samples from the Chinese Bohai Sea: implications for trophic transfer.Environ Sci Technol2016;50:4203-11

[56] Pittinger CA.Review of historical aquatic toxicity and bioconcentration data for the brominated flame retardant tetrabromobisphenol A (TBBPA): effects to fish, invertebrates, algae, and microbial communities.Environ Sci Pollut Res Int2018;25:14361-72

[57] Liu H,Zhang T.Pharmacokinetics and effects of tetrabromobisphenol a (TBBPA) to early life stages of zebrafish (Danio rerio).Chemosphere2018;190:243-52

[58] Groffen T,van Doorn L.Preliminary study on the distribution of metals and persistent organic pollutants (POPs), including perfluoroalkylated acids (PFAS), in the aquatic environment near Morogoro, Tanzania, and the potential health risks for humans.Environ Res2021;192:110299

[59] Xu H,Wang L.High throughput extraction strategy for simultaneous analysis of 19 tetrabromobisphenol A and halogenated carbazole analogs in seafood.Food Chem2021;350:129214

[60] Letcher RJ.High-sensitivity method for determination of tetrabromobisphenol-S and tetrabromobisphenol-A derivative flame retardants in great lakes herring gull eggs by liquid chromatography-atmospheric pressure photoionization-tandem mass spectrometry.Environ Sci Technol2010;44:8615-21

[61] de Jourdan, B. P.; Hanson, M. L.; Muir, D. C.; Solomon, K. R. Fathead minnow (Pimephales promelas Rafinesque) exposure to three novel brominated flame retardants in outdoor mesocosms: bioaccumulation and biotransformation.Environ Toxicol Chem2014;33:1148-55

[62] Liu A,Qu G,Shi J.Transformation/degradation of tetrabromobisphenol A and its derivatives: a review of the metabolism and metabolites.Environ Pollut2018;243:1141-53

[63] Kim SK,Oh JR.Characteristics of trophic transfer of polychlorinated biphenyls in marine organisms in Incheon North Harbor, Korea.Environ Toxicol Chem2002;21:834-41

[64] Harrad S,Rose NL,Davidson TA.Current-use brominated flame retardants in water, sediment, and fish from English lakes.Environ Sci Technol2009;43:9077-83

[65] Zhao J,Zhong Z.The bioaccumulation and biotransformation of tetrabromobisphenol A bis (allyl ether) in common carp (Cyprinus carpio).Environ Sci Pollut Res Int2023;30:121465-74

[66] Arnot JA.A review of bioconcentration factor (BCF) and bioaccumulation factor (BAF) assessments for organic chemicals in aquatic organisms.Environ Rev2006;14:257-97

[67] Burkhard LP,Embry MR.Comparing laboratory and field measured bioaccumulation endpoints.Integr Environ Assess Manag2012;8:17-31

[68] Gu SY,Kim HY.Brominated flame retardants in marine environment focused on aquaculture area: occurrence, source and bioaccumulation.Sci Total Environ2017;601-2:1182-91

[69] Yang Y,Gao Y.Identification and occurrence of TBBPA and its debromination and O-methylation transformation products in sediment, fish and whelks from a typical e-waste dismantling site.Sci Total Environ2022;833:155249

[70] Landrum PF.Influence of lipids on the bioaccumulation and trophic transfer of organic contaminants in aquatic organisms. In: Arts MT, Wainman BC, editors. Lipids in freshwater ecosystems. New York: Springer; 1999. pp. 203-34.

[71] Tang B,Luo XJ,Mai BX.Bioaccumulative characteristics of tetrabromobisphenol A and hexabromocyclododecanes in multi-tissues of prey and predator fish from an e-waste site, South China.Environ Sci Pollut Res Int2015;22:12011-7 PMCID:PMC4515246

[72] Fremlin KM,Letcher RJ,Gobas FAPC.Developing methods for assessing trophic magnification of perfluoroalkyl substances within an urban terrestrial avian food web.Environ Sci Technol2023;57:12806-18 PMCID:PMC10469464

[73] Ruan Y,Lu Y.Evaluating phospholipid- and protein-water partitioning of two groups of chemicals of emerging concern: diastereo- and enantioselectivity.J Hazard Mater2022;430:128499

[74] Zhang L,Low WV.Fugacity- and biotransformation-based mechanistic insights into the trophic transfer of organophosphate flame retardants in a subtropical coastal food web from the Northern Beibu Gulf of China.Water Res2024;261:122043

[75] Knutsen, H. K.; Åkesson, A.; Bampidis, V.; et al; EFSA Panel on Contaminants in the Food Chain (CONTAM). Update of the risk assessment of brominated phenols and their derivatives in food. EFSA. J. 2024, 22, e9034. PMCID:PMC11496907

[76] Yu Y,Xiang M,Kuang H.Potential obesogenic effects of TBBPA and its alternatives TBBPS and TCBPA revealed by metabolic perturbations in human hepatoma cells.Sci Total Environ2022;832:154847

[77] Barańska A,Mokra K.Genotoxic mechanism of action of TBBPA, TBBPS and selected bromophenols in human peripheral blood mononuclear cells.Front Immunol2022;13:869741 PMCID:PMC9039255

[78] Włuka A,Woźniak E.Tetrabromobisphenol A, terabromobisphenol S and other bromophenolic flame retardants cause cytotoxic effects and induce oxidative stress in human peripheral blood mononuclear cells (in vitro study).Chemosphere2020;261:127705

[79] Li S,Yin N,Zhang S.Developmental toxicity assessments for TBBPA and its commonly used analogs with a human embryonic stem cell liver differentiation model.Chemosphere2023;310:136924

[80] Sunday OE,Guanghua M.Review of the environmental occurrence, analytical techniques, degradation and toxicity of TBBPA and its derivatives.Environ Res2022;206:112594

[81] Lyche JL,Berge G.Human health risk associated with brominated flame-retardants (BFRs).Environ Int2015;74:170-80

[82] Ma J,Ma S,Li G.Temporal trends of “old” and “new” persistent halogenated organic pollutants in fish from the third largest freshwater lake in China during 2011-2018 and the associated health risks.Environ Pollut2020;267:115497

[83] Nøstbakken OJ,Rasinger JD.Factors influencing risk assessments of brominated flame-retardants; evidence based on seafood from the North East Atlantic Ocean.Environ Int2018;119:544-57

[84] Waiyarat S,Harrad S.In vitro estimation of oral bioaccessibility of brominated flame retardants in indoor dust by fasted and fed physiologically extraction test.J Environ Expo Assess2024;3:13

[85] Wikoff D,Perry C.Development of toxicity values and exposure estimates for tetrabromobisphenol A: application in a margin of exposure assessment.J Appl Toxicol2015;35:1292-308 PMCID:PMC6681068