Combined Effects of Temperature Changes and Bisphenol a on the Embryonic Development of Zebrafish (Danio rerio)
Main Article Content
Abstract
Water pollution by heat and organic matter is a global concern. Bisphenol A (BPA), an organic synthetic compound which is used as a raw material in the manufacture of many plastic products. It was found in water and has the potential to bioaccumulate and disrupt the endocrine system. This study evaluated the simultaneous influence of BPA and temperature changes on zebrafish embryos (Danio rerio). Embryos (0 day) were exposed in BPA (2.5 - 25 mg/L) at three temperature regimes: 23°C, 28°C (control) and 33°C. The amount of embryonic death, malformations (hematoma, pericardial edema) were recorded at 24 hours post fertilization (hpf), 48hpf, 72hpf and 96hpf. The results showed that embryo mortality and malformation rate increase depending on BPA concentration and temperature. At 96hpf endpoint, lethal concentration (LC50) and morphological effective concentration (mEC50) of 23°C, 28°C, 33°C were obtained as follows: LC50 = 14.886 mg/L and EC50 = 10.421 mg/L; LC50 = 16.732 mg/L and EC50 = 9.336 mg/L; LC50 = 7.627 mg/L and EC50 = 7.731 mg/L. The toxic of BPA at 33oC was higher that of control condition indicating the synergistic effect of BPA and temperature changes on the embryonic development of zebrafish. This suggests the climate change might also change the toxic effect of bisphenol A.
Keywords:
Bisphenol A, Danio rerio, Water pollution, Organic compound, Climate change.
References
[1] Coppola, L., & Rocca, C., Special Issue "Molecular Mechanisms of Bisphenol A Toxicity and Effects of Environmental Levels on Health”, International Journal of Molecular Sciences, Vol. 24, No. 9, 2023, https://doi.org/10.3390/ijms24098028.
[2] Wazir, U., & Mokbel, K., Bisphenol A: A Concise Review of Literature and a Discussion of Health and Regulatory Implications, In Vivo, Vol. 33, No. 5, 2019, pp. 1421-1423, https://doi.org/10.21873/invivo.11619.
[3] Vilarinho, F., Séndon, R., Kellen, A., Vaz, M., & Silva, A, Bisphenol A in food as a result of its migration from food packaging, Trends in Food Science & Technology, Vol. 91, 2019, pp. 33-65, https://doi.org/10.1016/J.TIFS.2019.06.012.
[4] Graziani, N., Carreras, H., & Wannaz, E. Atmospheric levels of BPA associated with particulate matter in an urban environment. Heliyon, Vol. 5, 2019, https://doi.org/10.1016/j.heliyon.2019.e01419.
[5] U.S. Environmental Protection Agency, Bisphenol A Action Plan, Vol. 22, 2010.
[6] Zhang, H., Zhang, Y., Li, J., & Yang, M., Occurrence and exposure assessment of bisphenol analogues in source water and drinking water in China, The Science of the total environment, Vol. 655, 2019, pp. 607-613, https://doi.org/10.1016/j.scitotenv.2018.11.053.
[7] Alammari, A., Khan, M., & Aqel, A., Trace identification of endocrine-disrupting bisphenol A in drinking water by solid-phase extraction and ultra-performance liquid chromatography-tandem mass spectrometry, Journal of King Saud University – Science, Vol. 2, 2020, pp. 1634-1640, https://doi.org/10.1016/j.jksus.2019.12.022.
[8] Yamazaki, E., Yamashita, N., Taniyasu, S., Lam, J., Lam, P., Moon, H., Jeong, Y., Kannan, P., Achyuthan, H., Munuswamy, N., & Kannan, K. Bisphenol A and other bisphenol analogues including BPS and BPF in surface water samples from Japan, China, Korea and India, Ecotoxicology and environmental safety, Vol. 122, 2015, pp. 565-72, https://doi.org/10.1016/j.ecoenv.2015.09.029.
[9] Xiao, C., Wang, L., Zhou, Q., & Huang, X., Hazards of bisphenol A (BPA) exposure: A systematic review of plant toxicology studies. Journal of hazardous materials, Vol. 384, 2020, https://doi.org/10.1016/j.jhazmat.2019.121488.
[10] Zaborowska, M., Wyszkowska, J., Borowik, A., & Kucharski, J., Bisphenol A—A Dangerous Pollutant Distorting the Biological Properties of Soil, International Journal of Molecular Sciences, Vol. 22, No. 23, 2021, https://doi.org/10.3390/ijms222312753.
[11] Vasiljevic, T., & Harner, T. Bisphenol A and its analogues in outdoor and indoor air: Properties, sources and global levels, The Science of the total environment, Vol. 789, 2021, https://doi.org/10.1016/J.SCITOTENV.2021.148013.
[12] Fan, X., Katuri, G., Caza, A., Rasmussen, P., & Kubwabo, C., Simultaneous measurement of 16 bisphenol A analogues in house dust and evaluation of two sampling techniques, Emerging Contaminants, Vol. 7, 2021, pp. 1-9, https://doi.org/10.1016/j.emcon.2020.12.001.
[13] Genuis, S., Beesoon, S., Birkholz, D., & Lobo, R., Human Excretion of Bisphenol A: Blood, Urine, and Sweat (BUS) Study, Journal of Environmental and Public Health, Vol. 2012, 2012, https://doi.org/10.1155/2012/185731.
[14] Chau, H., Kadokami, K., Duong, H., Kong, L., Nguyen, T., Nguyen, T., & Ito, Y., Occurrence of 1153 organic micropollutants in the aquatic environment of Vietnam, Environmental Science and Pollution Research, Vol. 25, No.8, 2018, pp. 7147-7156, https://doi.org/10.1007/s11356-015-5060-z.
[15] Guo, R., Du, Y., Zheng, F., Wang, J., Wang, Z., Ji, R., & Chen, J., Bioaccumulation and elimination of bisphenol a (BPA) in the alga Chlorella pyrenoidosa and the potential for trophic transfer to the rotifer Brachionus calyciflorus, Environmental pollution, Vol. 227, 2017, pp. 460-467, https://doi.org/10.1016/j.envpol.2017.05.010.
[16] Acconcia, F., Pallottini, V., & Marino, M., Molecular Mechanisms of Action of BPA, Dose-Response, Vol. 13, No. 4, 2015, https://doi.org/10.1177/1559325815610582.
[17] Naciff, J., Jump, M., Torontali, S., Carr, G., Tiesman, J., Overmann, G., & Daston, G., Gene expression profile induced by 17alpha-ethynyl estradiol, bisphenol A, and genistein in the developing female reproductive system of the rat, Toxicological sciences: an official journal of the Society of Toxicology, Vol. 68, No. 1, 2002, pp. 184-99, https://doi.org/10.1093/TOXSCI/68.1.184.
[18] Qiu, W., Liu, S., Chen, H., Luo, S., Xiong, Y., Wang, X., Xu, B., Zheng, C., & Wang, K., The comparative toxicities of BPA, BPB, BPS, BPF, and BPAF on the reproductive neuroendocrine system of zebrafish embryos and its mechanisms, Journal of hazardous materials, Vol. 406, 2021, https://doi.org/10.1016/j.jhazmat.2020.124303.
[19] Miller G.T. and Spoolman S., Essentials of ecology, 5th Eds, United States : Brooks/Cole Cengage Learning, Australia, 2009, pp. 58.
[20] Li, A., Leung, P., Bao, V., Lui, G., & Leung, K., Temperature-dependent physiological and biochemical responses of the marine medaka Oryzias melastigma with consideration of both low and high thermal extremes, Journal of Thermal Biology, Vol. 54, 2015, pp. 98-105, https://doi.org/10.1016/j.jtherbio.2014.09.011.
[21] Cao, X., & Corriveau, J., Migration of bisphenol A from polycarbonate baby and water bottles into water under severe conditions, Journal of agricultural and food chemistry, Vol. 56, No. 15, 2008, pp. 6378-6381, https://doi.org/10.1021/jf800870b.
[22] Lin, N., Ma, D., Liu, Z., Wang, X., & Ma, L., Migration of bisphenol A and its related compounds in canned seafood and dietary exposure estimation, Food Quality and Safety, Vol. 6, 2022, https://doi.org/10.1093/fqsafe/fyac006.
[23] Little, A., & Seebacher, F., Temperature determines toxicity: bisphenol A reduces thermal tolerance in fish, Environmental pollution, Vol. 197, 2015, pp. 84-89, https://doi.org/10.1016/j.envpol.2014.12.003.
[24] Holloway, G., Sibly, R., & Povey, S, Evolution in toxin-stressed environments. Functional Ecology, Vol. 4, No. 3, 1990, pp. 289-294, https://doi.org/10.2307/2389588.
[25] OECD, Test No. 236: Fish Embryo Acute Toxicity (FET) Test, OECD Guidelines for the Testing of Chemicals, Section 2, OECD Publishing, Paris, No. 236, 2013, https://doi.org/10.1787/20745761.
[26] OECD, Test No. 423: Acute Oral toxicity - Acute Toxic Class Method, OECD Guidelines for the Testing of Chemicals, Section 4, OECD Publishing, Paris, 2002, https://doi.org/10.1787/9789264071001-en.
[27] Scopel, C., Sousa, C., Machado, M., & Santos, W., BPA toxicity during development of zebrafish embryo, Brazilian Journal of Biology, Vol. 81, No. 2, 2021, https://doi.org/10.1590/1519-6984.230562.
[28] Maes, J., Verlooy, L., Buenafe, O., Witte, P., Esguerra, C., & Crawford, A, Evaluation of 14 Organic Solvents and Carriers for Screening Applications in Zebrafish Embryos and Larvae, PLoS ONE, Vol. 7, No. 10, 2012, https://doi.org/10.1371/journal.pone.0043850.
[29] Hallare, A., Nagel, K., Köhler, H., & Triebskorn, R., Comparative embryotoxicity and proteotoxicity of three carrier solvents to zebrafish (Danio rerio) embryos, Ecotoxicology and environmental safety, Vol. 63, No. 3, 2006, pp. 378-88, https://doi.org/10.1016/J.ECOENV.2005.07.006.
[30] Gyimah, E., Xu, H., Dong, X., Qiu, X., Zhang, Z., Bu, Y., & Akoto, O., Developmental neurotoxicity of low concentrations of bisphenol A and S exposure in zebrafish, Chemosphere, Vol. 262, 2021, https://doi.org/10.1016/j.chemosphere.2020.128045.
[31] Moreman, J., Lee, O., Trznadel, M., David, A., Kudoh, T., & Tyler, C., Acute Toxicity, Teratogenic, and Estrogenic Effects of Bisphenol A and Its Alternative Replacements Bisphenol S, Bisphenol F, and Bisphenol AF in Zebrafish Embryo-Larvae, Environmental science & technology, Vol. 51, No. 21, 2017, pp. 12796-12805, https://doi.org/10.1021/acs.est.7b03283.
[32] Reis, L., Lora-Benítez, A., Molina-López, A., Mora-Medina, R., Ayala-Soldado, N., & Moyano-Salvago, M., Evaluation of the Toxicity of Bisphenol A in Reproduction and Its Effect on Fertility and Embryonic Development in the Zebrafish (Danio rerio), International Journal of Environmental Research and Public Health, Vol. 19, 2022, https://doi.org/10.3390/ijerph19020962.
[33] Pype, C., Verbueken, E., Saad, M., Casteleyn, C., Ginneken, C., Knapen, D., & Cruchten, S., Incubation at 32.5°C and above causes malformations in the zebrafish embryo, Reproductive toxicology, Vol. 56, 2015, pp. 56-63, https://doi.org/10.1016/j.reprotox.2015.05.006
[2] Wazir, U., & Mokbel, K., Bisphenol A: A Concise Review of Literature and a Discussion of Health and Regulatory Implications, In Vivo, Vol. 33, No. 5, 2019, pp. 1421-1423, https://doi.org/10.21873/invivo.11619.
[3] Vilarinho, F., Séndon, R., Kellen, A., Vaz, M., & Silva, A, Bisphenol A in food as a result of its migration from food packaging, Trends in Food Science & Technology, Vol. 91, 2019, pp. 33-65, https://doi.org/10.1016/J.TIFS.2019.06.012.
[4] Graziani, N., Carreras, H., & Wannaz, E. Atmospheric levels of BPA associated with particulate matter in an urban environment. Heliyon, Vol. 5, 2019, https://doi.org/10.1016/j.heliyon.2019.e01419.
[5] U.S. Environmental Protection Agency, Bisphenol A Action Plan, Vol. 22, 2010.
[6] Zhang, H., Zhang, Y., Li, J., & Yang, M., Occurrence and exposure assessment of bisphenol analogues in source water and drinking water in China, The Science of the total environment, Vol. 655, 2019, pp. 607-613, https://doi.org/10.1016/j.scitotenv.2018.11.053.
[7] Alammari, A., Khan, M., & Aqel, A., Trace identification of endocrine-disrupting bisphenol A in drinking water by solid-phase extraction and ultra-performance liquid chromatography-tandem mass spectrometry, Journal of King Saud University – Science, Vol. 2, 2020, pp. 1634-1640, https://doi.org/10.1016/j.jksus.2019.12.022.
[8] Yamazaki, E., Yamashita, N., Taniyasu, S., Lam, J., Lam, P., Moon, H., Jeong, Y., Kannan, P., Achyuthan, H., Munuswamy, N., & Kannan, K. Bisphenol A and other bisphenol analogues including BPS and BPF in surface water samples from Japan, China, Korea and India, Ecotoxicology and environmental safety, Vol. 122, 2015, pp. 565-72, https://doi.org/10.1016/j.ecoenv.2015.09.029.
[9] Xiao, C., Wang, L., Zhou, Q., & Huang, X., Hazards of bisphenol A (BPA) exposure: A systematic review of plant toxicology studies. Journal of hazardous materials, Vol. 384, 2020, https://doi.org/10.1016/j.jhazmat.2019.121488.
[10] Zaborowska, M., Wyszkowska, J., Borowik, A., & Kucharski, J., Bisphenol A—A Dangerous Pollutant Distorting the Biological Properties of Soil, International Journal of Molecular Sciences, Vol. 22, No. 23, 2021, https://doi.org/10.3390/ijms222312753.
[11] Vasiljevic, T., & Harner, T. Bisphenol A and its analogues in outdoor and indoor air: Properties, sources and global levels, The Science of the total environment, Vol. 789, 2021, https://doi.org/10.1016/J.SCITOTENV.2021.148013.
[12] Fan, X., Katuri, G., Caza, A., Rasmussen, P., & Kubwabo, C., Simultaneous measurement of 16 bisphenol A analogues in house dust and evaluation of two sampling techniques, Emerging Contaminants, Vol. 7, 2021, pp. 1-9, https://doi.org/10.1016/j.emcon.2020.12.001.
[13] Genuis, S., Beesoon, S., Birkholz, D., & Lobo, R., Human Excretion of Bisphenol A: Blood, Urine, and Sweat (BUS) Study, Journal of Environmental and Public Health, Vol. 2012, 2012, https://doi.org/10.1155/2012/185731.
[14] Chau, H., Kadokami, K., Duong, H., Kong, L., Nguyen, T., Nguyen, T., & Ito, Y., Occurrence of 1153 organic micropollutants in the aquatic environment of Vietnam, Environmental Science and Pollution Research, Vol. 25, No.8, 2018, pp. 7147-7156, https://doi.org/10.1007/s11356-015-5060-z.
[15] Guo, R., Du, Y., Zheng, F., Wang, J., Wang, Z., Ji, R., & Chen, J., Bioaccumulation and elimination of bisphenol a (BPA) in the alga Chlorella pyrenoidosa and the potential for trophic transfer to the rotifer Brachionus calyciflorus, Environmental pollution, Vol. 227, 2017, pp. 460-467, https://doi.org/10.1016/j.envpol.2017.05.010.
[16] Acconcia, F., Pallottini, V., & Marino, M., Molecular Mechanisms of Action of BPA, Dose-Response, Vol. 13, No. 4, 2015, https://doi.org/10.1177/1559325815610582.
[17] Naciff, J., Jump, M., Torontali, S., Carr, G., Tiesman, J., Overmann, G., & Daston, G., Gene expression profile induced by 17alpha-ethynyl estradiol, bisphenol A, and genistein in the developing female reproductive system of the rat, Toxicological sciences: an official journal of the Society of Toxicology, Vol. 68, No. 1, 2002, pp. 184-99, https://doi.org/10.1093/TOXSCI/68.1.184.
[18] Qiu, W., Liu, S., Chen, H., Luo, S., Xiong, Y., Wang, X., Xu, B., Zheng, C., & Wang, K., The comparative toxicities of BPA, BPB, BPS, BPF, and BPAF on the reproductive neuroendocrine system of zebrafish embryos and its mechanisms, Journal of hazardous materials, Vol. 406, 2021, https://doi.org/10.1016/j.jhazmat.2020.124303.
[19] Miller G.T. and Spoolman S., Essentials of ecology, 5th Eds, United States : Brooks/Cole Cengage Learning, Australia, 2009, pp. 58.
[20] Li, A., Leung, P., Bao, V., Lui, G., & Leung, K., Temperature-dependent physiological and biochemical responses of the marine medaka Oryzias melastigma with consideration of both low and high thermal extremes, Journal of Thermal Biology, Vol. 54, 2015, pp. 98-105, https://doi.org/10.1016/j.jtherbio.2014.09.011.
[21] Cao, X., & Corriveau, J., Migration of bisphenol A from polycarbonate baby and water bottles into water under severe conditions, Journal of agricultural and food chemistry, Vol. 56, No. 15, 2008, pp. 6378-6381, https://doi.org/10.1021/jf800870b.
[22] Lin, N., Ma, D., Liu, Z., Wang, X., & Ma, L., Migration of bisphenol A and its related compounds in canned seafood and dietary exposure estimation, Food Quality and Safety, Vol. 6, 2022, https://doi.org/10.1093/fqsafe/fyac006.
[23] Little, A., & Seebacher, F., Temperature determines toxicity: bisphenol A reduces thermal tolerance in fish, Environmental pollution, Vol. 197, 2015, pp. 84-89, https://doi.org/10.1016/j.envpol.2014.12.003.
[24] Holloway, G., Sibly, R., & Povey, S, Evolution in toxin-stressed environments. Functional Ecology, Vol. 4, No. 3, 1990, pp. 289-294, https://doi.org/10.2307/2389588.
[25] OECD, Test No. 236: Fish Embryo Acute Toxicity (FET) Test, OECD Guidelines for the Testing of Chemicals, Section 2, OECD Publishing, Paris, No. 236, 2013, https://doi.org/10.1787/20745761.
[26] OECD, Test No. 423: Acute Oral toxicity - Acute Toxic Class Method, OECD Guidelines for the Testing of Chemicals, Section 4, OECD Publishing, Paris, 2002, https://doi.org/10.1787/9789264071001-en.
[27] Scopel, C., Sousa, C., Machado, M., & Santos, W., BPA toxicity during development of zebrafish embryo, Brazilian Journal of Biology, Vol. 81, No. 2, 2021, https://doi.org/10.1590/1519-6984.230562.
[28] Maes, J., Verlooy, L., Buenafe, O., Witte, P., Esguerra, C., & Crawford, A, Evaluation of 14 Organic Solvents and Carriers for Screening Applications in Zebrafish Embryos and Larvae, PLoS ONE, Vol. 7, No. 10, 2012, https://doi.org/10.1371/journal.pone.0043850.
[29] Hallare, A., Nagel, K., Köhler, H., & Triebskorn, R., Comparative embryotoxicity and proteotoxicity of three carrier solvents to zebrafish (Danio rerio) embryos, Ecotoxicology and environmental safety, Vol. 63, No. 3, 2006, pp. 378-88, https://doi.org/10.1016/J.ECOENV.2005.07.006.
[30] Gyimah, E., Xu, H., Dong, X., Qiu, X., Zhang, Z., Bu, Y., & Akoto, O., Developmental neurotoxicity of low concentrations of bisphenol A and S exposure in zebrafish, Chemosphere, Vol. 262, 2021, https://doi.org/10.1016/j.chemosphere.2020.128045.
[31] Moreman, J., Lee, O., Trznadel, M., David, A., Kudoh, T., & Tyler, C., Acute Toxicity, Teratogenic, and Estrogenic Effects of Bisphenol A and Its Alternative Replacements Bisphenol S, Bisphenol F, and Bisphenol AF in Zebrafish Embryo-Larvae, Environmental science & technology, Vol. 51, No. 21, 2017, pp. 12796-12805, https://doi.org/10.1021/acs.est.7b03283.
[32] Reis, L., Lora-Benítez, A., Molina-López, A., Mora-Medina, R., Ayala-Soldado, N., & Moyano-Salvago, M., Evaluation of the Toxicity of Bisphenol A in Reproduction and Its Effect on Fertility and Embryonic Development in the Zebrafish (Danio rerio), International Journal of Environmental Research and Public Health, Vol. 19, 2022, https://doi.org/10.3390/ijerph19020962.
[33] Pype, C., Verbueken, E., Saad, M., Casteleyn, C., Ginneken, C., Knapen, D., & Cruchten, S., Incubation at 32.5°C and above causes malformations in the zebrafish embryo, Reproductive toxicology, Vol. 56, 2015, pp. 56-63, https://doi.org/10.1016/j.reprotox.2015.05.006