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Identification of aquatic ecological risk of bisphenol S in four Asian countries based on the SSD and alternative toxicity data of model species Danio rerio

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Abstract

Bisphenol S (BPS), an organic compound and bisphenol analog, is commonly used as a substitute for bisphenol A. BPS is widely used in epoxy glues, can coatings, and thermal receipt papers; however, its risks have not been fully determined and the probability of its toxicity has been continuously suggested. In this study, we conducted BPS toxicity tests on aquatic plants (acute), cladocerans (acute and chronic), and fish (chronic) to determine its adverse effects, and calculated the toxicity values. Additionally, we conducted an ecological risk assessment of BPS in freshwater ecosystems with toxicity data from previous studies using the species sensitivity distribution method and BPS exposure data from 14 rivers in four countries in Asia (China, Japan, India, and South Korea). The chronic-based risk quotient (RQ) values of BPS in one river in China and two rivers in India were > 1, indicating a high ecological risk of BPS to aquatic organisms. The other four rivers in China showed medium ecological risk (0.1 < RQ < 1) and those in Japan and South Korea showed negligible chronic risk (RQ < 0.1) to aquatic organisms. We also suggest sensitive indicators in the model organism Danio rerio and highlighted the importance of the development of new method of ecological risk assessment. This study could provide new information that will assist in managing BPS and bisphenol analogs in freshwater ecosystems.

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All original data and code that support the findings of this study are available from the corresponding authors upon request.

References

  • ANZECC/ARMCANZ (2000) National Water Quality Management Strategy, Paper No. 4, Australian and New Zealand Guidelines for Fresh and Marine Water Quality, Volume 2. Aquatic Ecosystems

    Google Scholar 

  • Barron MG, Otter RR, Connors KA, Kienzler A, Embry MR (2021) Ecological thresholds of toxicological concern: a review. Front Toxicol 3:640183

    Google Scholar 

  • Basak S, Das MK, Duttaroy AK (2020) Plastics derived endocrine-disrupting compounds and their effects on early development. Birth Defects Res 112(17):1308–1325

    CAS  Google Scholar 

  • Brini E, Fennell CJ, Fernandez-Serra M, Hribar-Lee B, Lukšič M, Dill KA (2017) How water’s properties are encoded in its molecular structure and energies. Chem Rev 117:12385–12414

    CAS  Google Scholar 

  • ChemAnalyst (2021) Bisphenol S Market analysis: plant capacity, production, operating efficiency, technology, demand & supply, end-user industries, distribution channel, Regional Demand, 2015-2030. https://www.chemanalyst.com/industry-report/bisphenol-s-290

  • Chin KY, Pang KL, Mark-Lee WF (2018) A review on the effects of bisphenol A and its derivatives on skeletal health. Int J Med Sci 15(10):1043

    CAS  Google Scholar 

  • Cousins IT, Staples CA, Kleĉka GM, Mackay D (2002) A multimedia assessment of the environmental fate of bisphenol A. Hum Ecol Risk Assess 8:1107–1135

    Google Scholar 

  • Hernando MD, Mezcua M, Ferńandez-Alba AR, Barceló D (2006) Environmental risk assessment of pharmaceutical residues in wastewater effluents, surface waters and sediments. Talanta 69:334–342

    CAS  Google Scholar 

  • Herrero Ó, Aquilino M, Sánchez-Argüello P, Planelló R (2018) The BPA-substitute bisphenol S alters the transcription of genes related to endocrine, stress response and biotransformation pathways in the aquatic midge Chironomus riparius (Diptera, Chironomidae). PLoS One 13(2):e0193387

    Google Scholar 

  • Huang C, Wu L-H, Liu G-Q, Shi L, Guo Y (2018) Occurrence and ecological risk assessment of eight endocrine-disrupting chemicals in urban river water and sediments of south China. Arch Environ Contam Toxicol 75:224–235

    CAS  Google Scholar 

  • Ji K, Hong S, Kho Y, Choi K (2013) Effects of bisphenol S exposure on endocrine functions and reproduction of zebrafish. Environ Sci Technol 47(15):8793–8800

    CAS  Google Scholar 

  • Jin H, Zhu L (2016) Occurrence and partitioning of bisphenol analogues in water and sediment from Liaohe River Basin and Taihu Lake, China. Water Res 103:343–351

    CAS  Google Scholar 

  • Kuruto-Niwa R, Nozawa R, Miyakoshi T, Shiozawa T, Terao Y (2005) Estrogenic activity of alkylphenols, bisphenol S, and their chlorinated derivatives using a GFP expression system. Environ Toxicol Pharmacol 19(1):121–130

    CAS  Google Scholar 

  • Lee S, Liao C, Song GJ, Ra K, Kannan K, Moon HB (2015) Emission of bisphenol analogues including bisphenol A and bisphenol F from wastewater treatment plants in Korea. Chemosphere 119:1000–1006

    CAS  Google Scholar 

  • Lee J, Kho Y, Kim PG, Ji K (2018) Exposure to bisphenol S alters the expression of microRNA in male zebrafish. Toxicol Appl Pharmacol 338:191–196

    CAS  Google Scholar 

  • Lehmler HJ, Liu B, Gadogbe M, Bao W (2018) Exposure to bisphenol A, bisphenol F, and bisphenol S in US adults and children: the national health and nutrition examination survey 2013–2014. ACS omega 3(6):6523–6532

    CAS  Google Scholar 

  • Liao C, Liu F, Moon HB, Yamashita N, Yun S, Kannan K (2012) Bisphenol analogues in sediments from industrialized areas in the United States, Japan, and Korea: spatial and temporal distributions. Environ Sci Technol 46(21):11558–11565

    CAS  Google Scholar 

  • Li J, Li W, Huang X, Ding T (2021) Comparative study on the toxicity and removal of bisphenol S in two typical freshwater algae. Environ Sci Pollut Res 28:36861–36869

    CAS  Google Scholar 

  • Liu J, Zhang L, Lu G, Jiang R, Yan Z, Li Y (2021) Occurrence, toxicity and ecological risk of bisphenol A analogues in aquatic environment – a review. Ecotox Environ Safe 208:111481

    CAS  Google Scholar 

  • Mu X, Huang Y, Li X, Lei Y, Teng M, Li X, Wang C, Li Y (2018) Developmental effects and estrogenicity of bisphenol A alternatives in a zebrafish embryo model. Environ Sci Technol 52(5):3222–3231

    CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15(3):473–497

    CAS  Google Scholar 

  • Naderi M, Kwong RW (2020) A comprehensive review of the neurobehavioral effects of bisphenol S and the mechanisms of action: new insights from in vitro and in vivo models. Environ Int 145:106078

    CAS  Google Scholar 

  • Naderi M, Wong MY, Gholami F (2014) Developmental exposure of zebrafish (Danio rerio) to bisphenol-S impairs subsequent reproduction potential and hormonal balance in adults. Aquat Toxicol 148:195–203

    CAS  Google Scholar 

  • OECD (2004) OECD Guidelines for the testing of chemicals TG 202. Daphnia sp Acute Immobilization Test.

    Google Scholar 

  • OECD (2006) OECD Guidelines for the testing of chemicals TG 221. Lemna sp. growth inhibition test.

    Google Scholar 

  • OECD (2012) OECD Guidelines for the testing of chemicals TG 211. Daphnia magna Reproduction Test.

    Google Scholar 

  • OECD (2013) OECD Guidelines for the testing of chemicals TG 210. Fish, Early-life Stage Toxicity Test

    Google Scholar 

  • Park JC, Lee MC, Yoon DS, Han J, Kim M, Hwang UK, Jung JH, Lee JS (2018) Effects of bisphenol A and its analogs bisphenol F and S on life parameters, antioxidant system, and response of defensome in the marine rotifer Brachionus koreanus. Aquat Toxicol 199:21–29

    CAS  Google Scholar 

  • Park S, Hong Y, Lee J, Kho Y, Ji K (2019) Chronic effects of bisphenol S and bisphenol SIP on freshwater waterflea and ecological risk assessment. Ecotox Environ Safe 185:109694

    CAS  Google Scholar 

  • Qiu W, Zhao Y, Yang M, Farajzadeh M, Pan C, Wayne NL (2016) Actions of bisphenol A and bisphenol S on the reproductive neuroendocrine system during early development in zebrafish. Endocrinology 157(2):636–647

    CAS  Google Scholar 

  • Siracusa JS, Yin L, Measel E, Liang S, Yu X (2018) Effects of bisphenol A and its analogs on reproductive health: a mini review. Reprod Toxicol 79:96–123

    CAS  Google Scholar 

  • Song S, Song M, Zeng L, Wang T, Liu R, Ruan T, Jiang G (2014) Occurrence and profiles of bisphenol analogues in municipal sewage sludge in China. Environ Pollut 186:14–19

    CAS  Google Scholar 

  • Staples CA, Dorn PB, Klecka GM, O’Block ST, Harris LR (1998) A review of the environmental fate, effects, and exposures of bisphenol A. Chemosphere 36:2149–2173

    CAS  Google Scholar 

  • Thoene M, Dzika E, Gonkowski S, Wojtkiewicz J (2020) Bisphenol S in food causes hormonal and obesogenic effects comparable to or worse than bisphenol A: a literature review. Nutrients 12(2):532

    CAS  Google Scholar 

  • Ullah A, Pirzada M, Jahan S, Ullah H, Shaheen G, Rehman H, Siddiqui MF, Butt MA (2018a) Bisphenol A and its analogs bisphenol B, bisphenol F, and bisphenol S: comparative in vitro and in vivo studies on the sperms and testicular tissues of rats. Chemosphere 209:508–516

    CAS  Google Scholar 

  • Ullah A, Pirzada M, Jahan S, Ullah H, Turi N, Ullah W, Siddiqui MF, Zakria M, Lodhi KZ, Khan MM (2018b) Impact of low-dose chronic exposure to bisphenol A and its analogue bisphenol B, bisphenol F and bisphenol S on hypothalamo-pituitary-testicular activities in adult rats: a focus on the possible hormonal mode of action. Food Chem Toxicol 121:24–36

    CAS  Google Scholar 

  • Vasiljevic T, Harner T (2021) Bisphenol A and its analogues in outdoor and indoor air: properties, sources and global levels. Sci Total Environ 789:148013

    CAS  Google Scholar 

  • Vought V, Wang HS (2018) Impact of common environmental chemicals bisphenol A and bisphenol S on the physiology of Lumbriculus variegatus. Environ Toxicol Pharmacol 60:225–229

    CAS  Google Scholar 

  • Wang H, Feng CL, Guo GH, Zhang RQ, Liu YD, Wu FC (2013) Ecological risk assessment of bisphenol A in Chinese freshwaters. Huan Jing Ke Xue 34:2319–2328

    Google Scholar 

  • Wang W, Li Z, Zhang X, Zhang J, Ru S (2022) Bisphenol S impairs behaviors through disturbing endoplasmic reticulum function and reducing lipid levels in the brain of zebrafish. Environ Sci Technol

  • Wang W, Zhang X, Wang Z, Qin J, Wang W, Tian H, Ru S (2018) Bisphenol S induces obesogenic effects through deregulating lipid metabolism in zebrafish (Danio rerio) larvae. Chemosphere 199:286–296

    CAS  Google Scholar 

  • Wu LH, Zhang XM, Wang F, Gao CJ, Chen D, Palumbo JR, Guo Y, Zeng EY (2018) Occurrence of bisphenol S in the environment and implications for human exposure: A short review. Sci Total Environ 615:87–98

    CAS  Google Scholar 

  • Xue J, Kannan K (2019) Mass flows and removal of eight bisphenol analogs, bisphenol A diglycidyl ether and its derivatives in two wastewater treatment plants in New York State, USA. Sci Total Environ 648:442–449

    CAS  Google Scholar 

  • Yamazaki E, Yamashita N, Taniyasu S, Lam J, Lam PKS, Moon H-B, Jeong Y, Kannan P, Achyuthan H, Munuswamy N, Kannan K (2015) Bisphenol A and other bisphenol analogues including BPS and BPF in surface water samples from Japan, China, Korea and India. Ecotox Environ Safe 122:565–572

    CAS  Google Scholar 

  • Yang Y, Lu L, Zhang J, Yang Y, Wu Y, Shao B (2014) Simultaneous determination of seven bisphenols in environmental water and solid samples by liquid chromatography–electrospray tandem mass spectrometry. J Chromatogr A 1328:26–34

    CAS  Google Scholar 

  • Žalmanová T, Hošková K, Nevoral J, Prokešová Š, Zámostná K, Kott T, Petr J (2016) Bisphenol S instead of bisphenol A: a story of reproductive disruption by regretable substitution–a review. Czech J Anim Sci 61(10):433–449

    Google Scholar 

  • Zhang DH, Zhou EX, Yang ZL (2017) Waterborne exposure to BPS causes thyroid endocrine disruption in zebrafish larvae. PLoS One 12(5):e0176927

    Google Scholar 

  • Zhang L, Cheng Y, Qian Y, Ding T, Li J (2022) Phytotoxicity and accumulation of BPS to Pistia stratiotes under the influence of microplastics. Chemosphere 307:135854

    CAS  Google Scholar 

  • Zhang YF, Shan C, Wang Y, Qian LL, Jia DD, Zhang YF, Hao XD, Xu HM (2020) Cardiovascular toxicity and mechanism of bisphenol A and emerging risk of bisphenol S. Sci Total Environ 723:137952

    CAS  Google Scholar 

  • Zhao F, Jiang G, Wei P, Wang H, Ru S (2018) Bisphenol S exposure impairs glucose homeostasis in male zebrafish (Danio rerio). Ecotox Environ Safe 147:794–802

    CAS  Google Scholar 

  • Zhao X, Qui W, Zheng Y, Xiong J, Gao C, Hu S (2019) Occurrence, distribution, bioaccumulation, and ecological risk of bisphenol analogues, parabens and their metabolites in the Pearl River Estuary, South China. Ecotox Environ Safe 180:43–52

    CAS  Google Scholar 

  • Zheng C, Liu J, Ren J, Shen J, Fan J, Xi R, Chen W, Chen Q (2019) Occurrence, distribution and ecological risk of bisphenol analogues in the surface water from a water diversion project in Nanjing, China. Int J Env Res Pub He 16(18):3296

    CAS  Google Scholar 

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Funding

This work was supported by the Korea Institute of Toxicology (KIT; KK-2208-03, No. 1711159824).

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Author notes

  1. Yooeun Chae and Seonhee Bae contributed equally to this research.

Authors and Affiliations

  1. Ecological Risk Assessment Center, Gyeongnam Branch Institute, Korea Institute of Toxicology (KIT), Jinju, 52834, Republic of Korea

    Yooeun Chae, Seonhee Bae, Hi Gyu Moon & Sooyeon Kim

  2. Medical Industry Venture Center, Korea Testing Laboratory, Wonju, 26495, Republic of Korea

    Yong-Jae Kim

  3. Environmental Exposure & Toxicology Research Center, Korea Institute of Toxicology (KIT), Jinju, 52834, Republic of Korea

    Chang-Beom Park & June-Woo Park

  4. Environmental Safety-Assessment Center, Korea Institute of Toxicology (KIT), Jinju, 52834, Republic of Korea

    Dae-Wook Kim

  5. Gyeongnam Branch Institute, Korea Institute of Toxicology (KIT), Jinju, 52834, Republic of Korea

    Jong-Su Seo

Authors
  1. Yooeun Chae
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Contributions

Chae Y: writing—original draft preparation, data analysis. Bae S: writing—original draft preparation, data collection. Kim YJ: data collection, investigation. Park CB, Park JW, and Kim DW: material preparation. Moon HG, Kim S, and Seo JS: project administration, methodology, writing, reviewing and editing, supervision. All authors read and approved the final manuscript.

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Correspondence to Sooyeon Kim.

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Chae, Y., Bae, S., Moon, H.G. et al. Identification of aquatic ecological risk of bisphenol S in four Asian countries based on the SSD and alternative toxicity data of model species Danio rerio. Environ Sci Pollut Res 30, 77285–77298 (2023). https://doi.org/10.1007/s11356-023-27915-0

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