Estrogenic Activity and Endocrine Disruptor Compounds Determined in Guanabara Bay (Brazil) by Yeast Estrogen Screen Assays and Chemical Analyses

Autores

DOI:

https://doi.org/10.11137/1982-3908_2022_45_45450

Palavras-chave:

Micropollutants, HPLC, Acute toxicity

Resumo

Studies assessing the presence of endocrine disrupting compounds in marine environments have increased in the last decades. In Brazil, the combination of poor sanitation conditions and low investment in sewage treatment plants leads to significant contamination of receiving waters. The risks of these micropollutants in the aquatic biota include biochemical and histopathological alterations of the liver, gonads, and kidneys, as well as, reproductive process and development modifications, and behavioral changes, among others. The aim of this study was to evaluate the quality of the surface and deep waters of Guanabara Bay, southeastern Brazil, regarding the presence of estrogenic substances. Acute toxicity assays were also conducted employing Vibrio fischeri. The estrogenic activity of the water samples was determined by Yeast Estrogen Screen assay and the quantification of the Bisphenol A, estriol, 17β-estradiol, and 17α-ethinylestradiol by high-performance liquid chromatography, using fluorescence and diode array detectors. Estrogenic activity ranged from 9 to 77 ng L-1 of estradiol equivalents. The highest micropollutants concentrations were detected for bisphenol A (298.5 and 465.5 ng L-1), followed by 17α-ethinylestradiol (248 and 256.9 ng L-1), estriol (70.7 and 179.6 ng L-1), and 17β-estradiol (167 and 174.8 ng L-1) for surface and deep waters, respectively. The findings indicate significant risks for the Guanabara Bay ecosystem. No acute toxicity effects were observed in the V. fisheri assay. These data reflect the current environmental degradation situation of the bay’s waters and highlight the need for the systematic monitoring of this important estuary. 

Referências

Abdel-Khalek, A.A. 2018, 'Chronic exposure to water of Lake Qaroun induced metal-related testicular damage and endocrine disruption in male fish', Biological Trace Element Research, vol. 185, no. 1, pp. 197-204, DOI:10.1007/s12011-017-1220-y.

Amador, E.S.E. 2012, Bacia da Baía de Guanabara: características geoambientais, formação e ecossistemas, Interciência, Rio de Janeiro.

APHA, AWWA & WEF 2012, Standard methods for examination of water and wastewater, American Public Health Association, Washington.

Associação Brasileira de Normas Técnicas 2005, NBR 15411 Ecotoxicologia aquática – determinação do efeito inibitório de amostras de água sobre a emissão de luz de Vibrio fischeri (Ensaio de bactéria luminescente), ABNT, Rio de Janeiro.

Baptista Neto, J.A., Peixoto, T., Smith, B.J., Mcalister, J.J., Patchineelam, S.M., Patchineelam, S.R. & Fonseca, E.M. 2013, 'Geochronology and heavy metal flux to Guanabara Bay, Rio de Janeiro state: a preliminary study', Anais da Academia Brasileira de Ciências, vol. 85, no. 4, pp. 1317-27, DOI:10.1590/0001-3765201394612.

Baptista Neto, J.A., Rangel, C.M.A., Fonseca, E.M., Nascimento, M.T.L., Santos, A.D., Rodrigues, B.C.B. & De Melo, G.V. 2016, 'Concentrations and physicochemical speciation of heavy metals in urban runoff sediment from São Gonçalo-Rio de Janeiro/Brazil', Environmental Earth Sciences, vol. 75, no. 17, 1209, DOI: 10.1007/s12665-016-6000-z.

Baptista Neto, J.A.B., Gingele, F.X., Leipe, T. & Brehme, I. 2006, 'Spatial distribution of heavy metals in surficial sediments from Guanabara Bay: Rio de Janeiro, Brazil', Environmental Geology, vol. 49, no. 7, pp. 1051-63, DOI:10.1007/s00254-005-0149-1.

Beck, I.C., Bruhn, R. & Gandrass, J. 2006, 'Analysis of estrogenic activity in coastal surface waters of the Baltic Sea using the yeast estrogen screen', Chemosphere, vol. 63, no. 11, pp. 1870-78, DOI:10.1016/j.chemosphere.2005.10.022.

Caldwell, D.J., Mastrocco, F., Nowak, E., Johnston, J., Yekel, H., Pfeiffer, D. & Anderson, P.D. 2010, 'An assessment of potential exposure and risk from estrogens in drinking water', Environmental Health Perspectives, vol. 118, no. 3, pp. 338-44, DOI:10.1289/ehp.0900654.

Carreira, R.S., Wagener, A.L. & Readman, J.W. 2004, 'Sterols as markers of sewage contamination in a tropical urban estuary (Guanabara Bay, Brazil): space–time variations', Estuarine, Coastal and Shelf Science, vol. 60, no. 4, pp. 587-98, DOI:10.1016/j.ecss.2004.02.014.

Carvalho, M.C.N., Jayme, M.M., Arenazio, G.S., Araújo, F.V., Leite, S.G.F. & Aguila, E.M.D. 2016, 'Microbiological quality assessment by PCR and its antibiotic susceptibility in Mangrove Crabs (Ucides cordatus) from Guanabara Bay, Rio de Janeiro, Brazil', International Journal of Microbiology, vol. 1, pp. 1-9, DOI:10.1155/2016/7825031.

Cheng, J.R., Wang, K., Yu, J., Yu, Z.X., Yu, X.B. & Zhang, Z.Z. 2018, 'Distribution and fate modeling of 4-nonylphenol, 4-t-octylphenol, and bisphenol A in the Yong River of China', Chemosphere, vol. 195, pp. 594-605, DOI:10.1016/j.chemosphere.2017.12.085.

Chi, Y., Huang, Q., Zhang, H., Chen, Y. & Dong, S. 2016, 'In situ combined chemical and biological assessment of estrogenic pollution in a water recycling system', Journal of Environmental Sciences, vol. 43, pp. 216-23, DOI:10.1016/j.jes.2015.09.014.

Costa, C.R., Olivi, P., Botta, C.M. & Espindola, E.L. 2008, 'A toxicidade em ambientes aquáticos: discussão e métodos de avaliação', Química Nova, vol. 31, no. 7, pp.1820-30, DOI:10.1590/S0100-40422008000700038.

Cotrim, G., Fahning, C.S., da Rocha, G.O. & Hatje, V. 2016, 'Endocrine disruptors: strategies for determination and occurrence in marine environments', Journal of Integrated Coastal Zone Management, vol. 16, no. 3, pp. 1-29, DOI:10.5894/rgci669.

Cunha, D.L., Silva, S.M.C., Bila, D.M., Oliveira, J.L., Sarcinelli, P.N. & Larentis, A.L. 2016, 'Regulamentação do estrogênio sintético 17α-etinilestradiol em matrizes aquáticas na Europa, Estados Unidos e Brasil', Cadernos de Saúde Pública, vol. 32, no. 3, pp. 1-13, DOI:10.1590/0102-311X00056715.

Cunha, D.L., Silva, S.M.C., Nascimento, M.T.L., Felix, L., Gomes, G., Bila, D.M. & Fonseca, E.M. 2020, 'Occurrence of emerging contaminants and analysis of oestrogenic activity in the water and sediments from two coastal lagoons in south-eastern Brazil', Marine and Freshwater Research, vol. 72, no. 2, pp. 213-27, DOI:10.1071/MF19391.

Czarczyńska-Goślińska, B., Zgoła-Grześkowiak, A., Jeszka-Skowron, M., Frankowski, R. & Grześkowiak, T. 2017, 'Detection of bisphenol A, cumylphenol and parabens in surface waters of Greater Poland Voivodeship', Journal of Environmental Management, vol. 204, no. 1, pp. 50-60, DOI:10.1016/j.jenvman.2017.08.034.

De Carvalho, D.G. & Baptista Neto, J.A. 2016, 'Microplastic pollution of the beaches of Guanabara Bay, Southeast Brazil', Ocean & Coastal Management, vol. 128, pp. 10-7, DOI:10.1016/j.ocecoaman.2016.04.009.

Dias, A.C.V., Gomes, F.W., Bila, D.M., Sant’Anna Jr, G.L. & Dezotti, M. 2015, 'Analysis of estrogenic activity in environmental waters in Rio de Janeiro state (Brazil) using the yeast estrogen screen', Ecotoxicology and Environmental Safety, vol. 120, pp. 41-7, DOI:10.1016/j.ecoenv.2015.05.013.

European Commission Directive 2013, 2013/39/EU of the European Parliament Amending Directives 2000/60/EC as Regards Priority Substances in the Field of Water Policy, viewed 13 December 2020, <https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2013:226:0001:0017:en:PDF>.

Fernandez, M.A., Wagener, A.D.L.R., Limaverde, A.M., Scofield, A.D.L., Pinheiro, F. M. & Rodrigues, E. 2005, 'Imposex and surface sediment speciation: a combined approach to evaluate organotin contamination in Guanabara Bay, Rio de Janeiro, Brazil', Marine Environmental Research, vol. 59, no. 5, pp. 435-52, DOI:10.1016/j.marenvres.2004.07.001.

Ferreira, A.P., Horta, M.A.P. & Cunha, C.L.N. 2010, 'Assessment of heavy metal concentrations in sediment, water and organs of Nycticorax nycticorax (Black-crowned Night Heron) in Sepetiba Bay, Rio de Janeiro, Brazil', Journal of Integrated Coastal Zone Management, vol. 10, no. 2, pp. 81-93, DOI:10.1007/s10646-007-0143-3.

Fistarol, G.O., Coutinho, F.H., Moreira, A.P.B., Venas, T., Cánovas, A., de Paula Jr, S. E. & Paranhos, R. 2015, 'Environmental and sanitary conditions of Guanabara Bay, Rio de Janeiro', Frontiers in Microbiology, vol. 6, no. 1232, pp. 1-17, DOI:10.3389/fmicb.2015.01232.

Fonseca, E.M., Baptista Neto, J.A., Silva, C.G., McAlister, J.J., Smith, B.J. & Fernandez, M.A. 2013, 'Stormwater impact in Guanabara Bay (Rio de Janeiro): evidences of seasonal variability in the dynamic of the sediment heavy metals', Estuarine, Coastal and Shelf Science, vol. 130, pp. 161-8, DOI:10.1016/j.ecss.2013.04.022.

Francioni, E., Wagener, A., Scofield, A.L. & Cavalier, B. 2005, 'Biomonitoring of polycyclic aromatic hydrocarbon in Perna perna from Guanabara Bay, Brazil', Environmental Forensics, vol. 6, no. 4, pp. 361-70, DOI:10.1080/15275920500351759.

Frische, T., Faust, M., Meyer, W. & Backhaus, T. 2009, 'Toxic masking and synergistic modulation of the estrogenic activity of chemical mixtures in a yeast estrogen screen (YES)', Environmental Science and Pollution Research, vol. 16, no. 5, pp. 593-603, DOI:10.1007/s11356-009-0184-7.

Gilbert, N. 2012, 'Drug-pollution law all washed up', Nature, vol. 491, no. 7425, pp. 503-4, DOI:10.1038/491503a.

Gu, Y., Yu, J., Hu, X. & Yin, D. 2016, 'Characteristics of the alkylphenol and bisphenol A distributions in marine organisms and implications for human health: A case study of the East China Sea', Science of the Total Environment, vol. 539, pp. 460-9, DOI:10.1016/j.scitotenv.2015.09.011.

Huang, F., Karu, K. & Campos, L.C. 2021, 'Simultaneous measurement of free and conjugated estrogens in surface water using capillary liquid chromatography tandem mass spectrometry', Analyst, vol. 146, no. 8, pp. 2689-704, DOI:10.1039/D0AN02335C.

Ismail, N.A.H, Wee, S.Y, Kamarulzaman, N.H & Aris, A.Z. 2019, 'Quantification of multi-classes of endocrine-disrupting compounds in estuarine water', Environmental Pollution, vol. 249, pp. 1019-28, DOI:10.1016/j.envpol.2019.03.089.

Kahru, A., Kurvet, M. & Külm, I. 1996, 'Toxicity of phenolic wastewater to luminescent bacteria Photobacterium phosphoreum and activated sludges', Water Science and Technology, vol. 33, no. 6, pp. 139-46, DOI:10.2166/wst.1996.0090.

Kang, J. H. & Kondo, F. 2005, 'Bisphenol A degradation in seawater is different from that in river water', Chemosphere, vol. 60, no. 9, pp. 1288-92, DOI:10.1016/j.chemosphere.2005.01.058.

Kunz, P.Y., Simon, E., Creusot, N., Jayasinghe, B.S., Kienle, C., Maletz, S. & Hollert, H. 2017, 'Effect-based tools for monitoring estrogenic mixtures: evaluation of five in vitro bioassays', Water Research, vol. 110, pp. 378-88, DOI:10.1016/j.watres.2016.10.062.

Li, S., Sun, Q., Wu, Q., Gui, W., Zhu, G. & Schlenk, D. 2019, 'Endocrine disrupting effects of tebuconazole on different life stages of zebrafish (Danio rerio)', Environmental Pollution, vol. 249, pp. 1049-59, DOI:10.1016/j.envpol.2019.03.067.

Li, Y., Yang, L., Zhen, H., Chen, X., Sheng, M., Li, K. & Cao, G. 2021, 'Determination of estrogens and estrogen mimics by solid-phase extraction with liquid chromatography-tandem mass spectrometry', Journal of Chromatography B, vol. 1168, 122559, DOI:10.1016/j.jchromb.2021.122559.

Liu, G., Ke, M., Fan, X., Zhang, M., Zhu, Y., Lu, T. & Qian, H. 2018, 'Reproductive and endocrine-disrupting toxicity of Microcystis aeruginosa in female zebrafish', Chemosphere, vol. 192, pp. 289-96, DOI:10.1016/j.chemosphere.2017.10.167.

Locatelli, M., Sciascia, F., Cifelli, R., Malatesta, L., Bruni, P. & Croce, F. 2016, 'Analytical methods for the endocrine disruptor compounds determination in environmental water samples', Journal of Chromatography A, vol. 1434, pp. 1-18, DOI:10.1016/j.chroma.2016.01.034.

Melo, G.V., Baptista Neto, J.A., Malm, O., Fernandez, M.A. & Patchineelam, S.M. 2015, 'Composition and behaviour of heavy metals in suspended sediments in a tropical estuarine system', Environmental Earth Sciences, vol. 73, no. 3, pp. 133-44, DOI:10.1007/s12665-014-3491-3.

Miret, N.V., Pontillo, C.A., Zárate, L.V., de Pisarev, D.K., Cocca, C. & Randi, A.S. 2019, 'Impact of endocrine disruptor hexachlorobenzene on the mammary gland and breast cancer: The story thus far', Environmental Research, vol. 173, pp. 330-41, DOI:10.1016/j.envres.2019.03.054.

Montagner, C.C., Vidal, C. & Acayaba, R.D. 2017, 'Contaminantes emergentes em matrizes aquáticas do Brasil: cenário atual e aspectos analíticos, ecotoxicológicos e regulatórios', Química Nova, vol. 40, no. 9, pp. 1094-110, DOI:10.21577/0100-4042.20170091.

Nascimento, M.T.L., Santos, A.D., Felix, L.C., Gomes, G., Sá, M.D.O., Cunha, D.L. & Bila, D.M. 2018, 'Determination of water quality, toxicity and estrogenic activity in a nearshore marine environment in Rio de Janeiro, Southeastern Brazil', Ecotoxicology and Environmental Safety, vol. 149, pp. 197-202, DOI:10.1016/j.ecoenv.2017.11.045.

Negintaji, A., Safahieh, A., Zolgharnein, H. & Matroodi, S. 2018, 'Short-term induction of vitellogenesis in the immature male yellowfin seabream (Acanthopagrus latus) exposed to bisphenol A and 17 β-estradiol', Toxicology and Industrial Health, vol. 34, no. 2, pp. 119-27, DOI:10.1177/0748233717748099.

Nimer, E. 1989, Climatologia do Brasil, 2nd edn, IBGE, Departamento de Recursos Naturais e Estudos Ambientais, Rio de Janeiro, viewed 10 January 2020, <https://biblioteca.ibge.gov.br/visualizacao/livros/liv81099.pdf>.

Porseryd, T., Kellner, M., Caspillo, N.R., Volkova, K., Elabbas, L., Ullah, S. & Hällström, I.P. 2017, 'Combinatory effects of low concentrations of 17α-etinylestradiol and citalopram on non-reproductive behavior in adult zebrafish (Danio rerio)', Aquatic Toxicology, vol. 193, pp. 9-17, DOI:10.1016/j.aquatox.2017.10.001.

Rao, K., Lei, B., Li, N., Ma, M. & Wang, Z. 2013, 'Determination of estrogens and estrogenic activities in water from three rivers in Tianjin, China', Journal of Environmental Sciences, vol. 25, no. 6, pp. 1164-71, DOI:10.1016/S1001-0742(12)60149-1.

Rocha, B.A., Asimakopoulos, A.G., Honda, M., da Costa, N.L., Barbosa, R.M., Barbosa, F. & Kannan, K. 2018, 'Advanced data mining approaches in the assessment of urinary concentrations of bisphenols, chlorophenols, parabens and benzophenones in Brazilian children and their association to DNA damage', Environment International, vol. 116, pp. 269-77, DOI:10.1016/j.envint.2018.04.023.

Routledge, E.J. & Sumpter, J.P. 1996, 'Estrogenic activity of surfactants and some of their degradation products assessed using a recombinant yeast screen', Environmental Toxicology and Chemistry, vol. 15, no. 3, pp. 241-48, DOI:10.1002/etc.5620150303.

SCHER - vide Scientific Committee on Health and Environmental Risks 2011, Environmental Quality Standards - 17β-estradiol (E2), viewed 9 December 2021, <https://ec.europa.eu/health/scientific_committees/environmental_risks/docs/scher_o_13pdf>.

Selvaraj, K.K., Shanmugam, G., Sampath, S., Larsson, D.J. & Ramaswamy, B.R. 2014, 'GC–MS determination of bisphenol A and alkylphenol ethoxylates in river water from India and their ecotoxicological risk assessment', Ecotoxicology and Environmental Safety, vol. 99, pp. 13-20, DOI:10.1016/j.ecoenv.2013.09.006.

Shi, J., Liu, X., Chen, Q. & Zhang, H. 2014, 'Spatial and seasonal distributions of estrogens and bisphenol A in the Yangtze River Estuary and the adjacent East China Sea', Chemosphere, vol. 111, pp. 336-43, DOI:10.1016/j.chemosphere.2014.04.046.

Silva, A.M.F., Lemes, V.R.R., Barretto, H.H.C., Oliveira, E.S., de Alleluia, I.B. & Paumgartten, F.J.R. 2003, 'Polychlorinated biphenyls and organochlorine pesticides in edible fish species and dolphins from Guanabara Bay, Rio de Janeiro, Brazil', Bulletin of Environmental Contamination and Toxicology, vol. 70, no. 6, pp. 1151-57, DOI:10.1007/s00128-003-0102-5.

Silva, F.S., Bitencourt, J.A.P., Savergnini, F., Guerra, L.V., Baptista-Neto, J.A. & Crapez, M.A.C. 2011, 'Bioavailability of organic matter in the superficial sediment of Guanabara Bay, Rio de Janeiro, Brazil', Anuario do Instituto de Geociencias, vol. 34, no. 1, pp. 52-63, DOI:10.11137/2011_1_52-63.

Silva, M.A.M., Silva, A.L.C., Santos, C.L., Silvestre, CP. & Antonio, R.V.M. 2016, 'The Beaches of Guanabara Bay in Rio de Janeiro State', Revista Brasileira de Geomorfologia, vol. 17, no. 2, pp. 205-25, DOI:10.20502/rbg.v17i2.839.

Soares-Gomes, A., Da Gama, B.A.P., Baptista Neto, J.A., Freire, D.G., Cordeiro, R.C., Machado, W. & Pereira, R.C. 2016, 'An environmental overview of Guanabara Bay, Rio de Janeiro', Regional Studies in Marine Science, vol. 8, no. 2, pp. 319-30, DOI:10.1016/j.rsma.2016.01.009.

Solaun, O., Rodríguez, J.G., Menchaca, I., López-García, E., Martínez, E., Zonja, B. & Larreta, J. 2021, 'Contaminants of emerging concern in the Basque coast (N Spain): Occurrence and risk assessment for a better monitoring and management decisions', Science of the Total Environment, vol. 765, 142765, DOI:10.1016/j.scitotenv.2020.142765.

Truter, J.C., Wyk, J.V. & Newman, B.K. 2015, 'In vitro screening for endocrine disruptive activity in selected South African harbours and river mouths', African Journal of Marine Science, vol. 37, no. 4, pp. 567-74, DOI:10.2989/1814232X.2015.1105296.

Viganò, L., Benfenati, E., Van Cauwenberge, A., Eidem, J.K., Erratico, C., Goksøyr, A. & Urbatzka, R. 2008, 'Estrogenicity profile and estrogenic compounds determined in river sediments by chemical analysis, ELISA and yeast assays', Chemosphere, vol. 73, no. 7, pp. 1078-89, DOI:10.1016/j.chemosphere.2008.07.057.

Xavier, D.B.A., De Andrade, B.I. & Moreira, I. 2002, 'Chlorinated pesticides in mussels from Guanabara Bay, Rio de Janeiro, Brazil', Marine Pollution Bulletin, vol. 44, no. 1, pp. 79-81, DOI:10.1016/s0025-326x(01)00222-3.

Yamazaki, E., Yamashita, N., Taniyasu, S., Lam, J., Lam, P.K., Moon, H.B. & Kannan, K. 2015, '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, pp. 565-72, DOI:10.1016/j.ecoenv.2015.09.029.

Zhao, J.L., Ying, G.G., Chen, F., Liu, Y.S., Wang, L., Yang, B. & Tao, R. 2011, 'Estrogenic activity profiles and risks in surface waters and sediments of the Pearl River system in South China assessed by chemical analysis and in vitro bioassay', Journal of Environmental Monitoring, vol. 13, no. 4, pp. 813-21, DOI:10.1039/c0em00473a.

Zhong, R., Zou, H., Gao, J., Wang, T., Bu, Q, Wang, Z. L. & Wang, Z. 2021, 'A critical review on the distribution and ecological risk assessment of steroid hormones in the environment in China', Science of the Total Environment, vol. 786, 147452, DOI:10.1016/j.scitotenv.2021.147452.

Anuário do Instituto de Geociências volume 45. Ano 2022

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2022-07-14

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v. 45 (2022)

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Ciências do Ambiente

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