Emerging contaminant occurrence and toxic effects on zebrafish embryos to assess the adverse effects caused by mixtures of substances in the environment

Martini, Gisela de Assis; Montagner, Cassiana Carolina; Viveiros, William; Quinaglia, Gilson Alves; França, Daniela Dayrell; Munin, Nívea Cristina Guedes; Lopes-Ferreira, Mônica; Rogero, Sizue Ota; Rogero, José Roberto

doi:10.1007/s11356-020-11963-x

Research Article
Published: 06 January 2021

Emerging contaminant occurrence and toxic effects on zebrafish embryos to assess the adverse effects caused by mixtures of substances in the environment

Gisela de Assis Martini ORCID: orcid.org/0000-0002-5173-8705¹,
Cassiana Carolina Montagner²,
William Viveiros³,
Gilson Alves Quinaglia³,
Daniela Dayrell França³,
Nívea Cristina Guedes Munin^2,5,
Mônica Lopes-Ferreira⁴,
Sizue Ota Rogero¹ &
José Roberto Rogero¹

Environmental Science and Pollution Research volume 28, pages 20313–20329 (2021)Cite this article

465 Accesses
1 Altmetric
Metrics details

Abstract

The contaminants of emerging concern (CECs) have been receiving global attention due to their worldwide presence in water bodies. The CECs could be originated from synthetic or natural sources, and they are not commonly monitored, although these substances are continuously reaching the aquatic environment. The main goal of this study was to determine the occurrence of some target CECs in São Paulo state surface water, once there is practically no information on the presence and concentration range of these substances at the studied sites. In addition, the present study aimed to assess adverse effects in the non-target fish embryo of Danio rerio (zebrafish) after exposure to surface water organic extract samples during 96 h using FET test. The CECs in surface water samples were determined by solid-phase extraction and liquid chromatography coupled by mass spectrometry. A 2-year study was assessed in 7 rivers and 3 reservoirs at São Paulo state, where 25 of the 30 analyzed substances were quantified, being caffeine the substance with the highest concentration range (5.5 ng L⁻¹ to 69 μg L⁻¹) and detected in 95% of analyzed samples, followed by bisphenol A (6.5–1300 ng L⁻¹) and carbendazim (4.7–285 ng L⁻¹), found in 50% and 85% of the analyzed samples, respectively. The chemical analysis and biological test were not performed in order to show a direct relationship between concentrations and observed effects on embryos; however, the combined approach can provide a better understanding of the adverse effects caused by mixtures of substances at relevant environmental concentrations. Regarding the adverse effects, it was observed that in the samples from sites with higher anthropogenic activity in the surroundings, there was also a higher mortality rate in organisms. At the Ribeirão Pires River and Sapucaí-Guaçu River, the mortality rate during the 2-year study was 21.6% and 9.3%, respectively. The morphological abnormality rates were higher at Ribeirão Grande (21.4%) and Ribeirão Pires (29.5%) Rivers. The obtained results aim to show that even in low concentrations (ng–μg L⁻¹) the CECs can cause adverse effects on non-target species, and because of that, new chemical indicators would be important to monitor the water quality and protect the aquatic biota.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Data availability

The obtained and analyzed data of this study are included in this article and on the supplementary information files.

References

Acir IH, Guenther K (2018) Endocrine-disrupting metabolites of alkylphenol ethoxylates – a critical review of analytical methods, environmental occurrences, toxicity, and regulation. Sci Tot Environ 635:1530–1546. https://doi.org/10.1016/j.scitotenv.2018.04.079
CAS Article Google Scholar
Aeppli C, Berg M, Hofstetter TB, Kipfer R, Schwarzenbach RP (2008) Simultaneous quantification of polar and non-polar volatile organic compounds in water samples by direct aqueous injection-gas chromatography/mass spectrometry. J Chromat A. 1181(1–2):116–124. https://doi.org/10.1016/j.chroma.2007.12.043
CAS Article Google Scholar
Albuquerque AF, Ribeiro JS, Kummrow F, Nogueira AJA, Montagner CC, Umbuzeiro GA (2016) Pesticides in Brazilian freshwaters: a critical review. Environ Sci: Processes Impacts 18:779–787. https://doi.org/10.1039/C6EM00268D
CAS Article Google Scholar
Altenburger R, Walter H, Grote M (2004) What contributes to the combined effect of a complex mixture? Environ Sci Technol 38:6353–6362. https://doi.org/10.1021/es049528k
CAS Article Google Scholar
Bahlmann A, Carvalho JJ, Weller MG, Panne U, Schneider RJ (2012) Immunoassays as high-throughput tools: monitoring spatial and temporal variations of carbamazepine, caffeine and cetirizine in surface and wastewaters. Chemosphere. 89(11):1278–1286. https://doi.org/10.1016/j.chemosphere.2012.05.020
CAS Article Google Scholar
Barceló D, Petrović M, Eljarrat E, de Alda MJL, Kampioti A (2004) Chapter 21 Environmental analysis. Editor(s): E. Heftmann. J. Chromatogr. Libr., Elsevier. 69(Part B):987-1036. https://doi.org/10.1016/S0301-4770(04)80034-4
Barnes KK, Kolpin DW, Furlong ET, Zaugg SD, Meyer MT, Barber LB (2008) A national reconnaissance of pharmaceuticals and other organic wastewater contaminants in the United States — I groundwater. Sci. Tot. Environ. 402(2–3):192–200. https://doi.org/10.1016/j.scitotenv.2008.04.028
CAS Article Google Scholar
Bergman A, Becher G, Blumberg B, Bjerregaard P, Bornman, Brandt I, Casey SC, Frouin H, Giudice LC, Heindel JJ, Iguchi T, Jobling S, Kidd KA, Kortenkamp A, Lind PM, Muir D, Ochieng R, Ropstad E, Ross PS, Skakkebaek EN, Toppari J, Vandenberg LN, Woodruff TJ, Zoeller RT (2015) Manufacturing doubt about endocrine disrupter science – a rebuttal of industry-sponsored critical comments on the UNEP/WHO report “State of the Science of Endocrine Disrupting Chemicals 2012”. Regul Toxicol Pharmacol 73(3):1007–1017. https://doi.org/10.1016/j.yrtph.2015.07.026
Article Google Scholar
Bilal M, Adeel M, Rasheed T, Zhao Y, Iqbal HMN (2019) Emerging contaminants of high concern and their enzyme-assisted biodegradation – a review. Environ Int 124:336–353. https://doi.org/10.1016/j.envint.2019.01.011
CAS Article Google Scholar
Braunbeck T, Kais B, Lammer E, Otte J, Schneider K, Stengel D, Strecker R (2015) The fish embryo test (FET): origin, applications, and future. Environ Sci Pollut Res 22:16247–16261. https://doi.org/10.1007/s11356-014-3814-7
CAS Article Google Scholar
Brix R, Noguerol TN, Piña B, Balaam J, Nilsen AJ, Tollefsen KE, Levy W, Schramm KW, Barceló D (2010) Evaluation of the suitability of recombinant yeast-based estrogenicity assays as a pre-screening tool in environmental samples. Environ Int 36(4):361–367. https://doi.org/10.1016/j.envint.2010.02.004
CAS Article Google Scholar
Brown AR, Green JM, Moreman J, Gunnarsson LM, Mourabit S, Ball J, Winter MJ, Trznadel M, Correia A, Hacker C, Perry A, Wood ME, Hetheridge MJ, Currie RA, Tyler CR (2019) Cardiovascular effects and molecular mechanisms of bisphenol A and its metabolite MBP in Zebrafish. Environ Sci Technol 53(1):463–474. https://doi.org/10.1021/acs.est.8b04281
Buerge II, Poiger T, Müller MD, Buser HR (2003) Caffeine, an anthropogenic marker for wastewater contamination of surface waters. Environ Sci Technol 37(4):691–700. https://doi.org/10.1021/es020125z
CAS Article Google Scholar
Caldas SS, Bolzan CM, Guilherme JR, Silveira MAK, Escarrone ALV, Primel EG (2013) Determination of pharmaceuticals, personal care products, and pesticides in surface and treated waters: method development and survey. Environ Sci Pollut Res Int 20(8):5855–5863. https://doi.org/10.1007/s11356-013-1650-9
CAS Article Google Scholar
Careghini A, Saponaro S, Sezenna E, Daghio M, Franzetti A, Gandolfi I, Bestetti G (2015) Lab-scale tests and numerical simulations for in situ treatment of polluted groundwater. J Haz Mat 287:162–170. https://doi.org/10.1016/j.jhazmat.2015.01.028
CAS Article Google Scholar
Chen HY, Huang YH, Wen CC, Wang YH, Chen WL, Chen LC, Tsay HJ (2008) Movement disorder and neuromuscular change in zebrafish embryos after exposure to caffeine. Neurotoxicol Teratol 30(5):440–447. https://doi.org/10.1016/j.ntt.2008.04.003
CAS Article Google Scholar
Chen W, Lau S, Fan Y, Wu RSS, Ge W (2017) Juvenile exposure to bisphenol A promotes ovarian differentiation but suppresses its growth – potential involvement of pituitary follicle-stimulating hormone. Aquat Toxicol 193:111–121. https://doi.org/10.1016/j.aquatox.2017.10.008
CAS Article Google Scholar
Cleary JA, Tillitt DE, vom Saal FS, Nicks DK, Claunch RA, Bhandari RK (2019) Atrazine induced transgenerational reproductive effects in medaka (Oryzias latipes). Environ Pol 251:639–650. https://doi.org/10.1016/j.envpol.2019.05.013
CAS Article Google Scholar
Colman JR, Baldwin D, Johnson LL, Scholz NL (2009) Effects of the synthetic estrogen, 17α-ethinylestradiol, on aggression and courtship behavior in male zebrafish (Danio rerio). Aquat Toxicol 91(4):346–354. https://doi.org/10.1016/j.aquatox.2008.12.001
CAS Article Google Scholar
Cortez FS, Pereira CDS, Santos AR, Cesar A, Choueri RB, Martini GA, Bohrer-Morel MB (2012) Biological effects of environmentally relevant concentrations of the pharmaceutical triclosan in the marine mussel Perna perna (Linnaeus, 1758). Env Pol 168:145–150. https://doi.org/10.1016/j.envpol.2012.04.024
CAS Article Google Scholar
Deere JR, Moore S, Ferrey M, Jankowski MD, Primus A, Convertino M, Servadio JL, Phelps NBD, Hamilton MC, Chenaux-Ibrahim Y, Travis DA, Wolf TM (2020) Occurrence of contaminants of emerging concern in aquatic ecosystems utilized by Minnesota tribal communities. Sci. Tot. Environ. 724(1):38–57. https://doi.org/10.1016/j.scitotenv.2020.138057
CAS Article Google Scholar
Di Paolo C, Ottermanns R, Keiter S, Ait-Aissa S, Bluhm K, Brack W, Breitholtz M, Buchinger S, Carere M, Chalon C, Cousin X, Dulio V, Escher BI, Hamers T, Hilscherová K, Jarque S, Jonas A, Maillot-Marechal E, Marneffe Y, Nguyen MT, Pandard P, Schifferli A, Schulze T, Seidensticker S, Seiler TB, Tang J, van der Oost J, Vermeirssen J, Zounková R, Zwart N, Hollert H (2016) Bioassay battery interlaboratory investigation of emerging contaminants in spiked water extracts – towards the implementation of bioanalytical monitoring tools in water quality assessment and monitoring. Water Res 104:473–484. https://doi.org/10.1016/j.watres.2016.08.018
CAS Article Google Scholar
EC - Environment Canada: Biological test method for toxicity tests using early life stages of rainbow trout: front matter (2014) https://www.canada.ca/en/environment-climate-change/services/wildlife-research-landscape-science/biological-test-method-publications/toxicity-rainbow-trout/front-matter.html
EFSA – Opinion of the Scientific Panel on Animal Health and Welfare on a request from the Commission related to the aspects of the biology and welfare of animals used for experimental and other scientific purposes (EFSA-Q-2004-105) (2005) EFSA J 292:1–46. https://doi.org/10.2903/j.efsa.2005.292
Article Google Scholar
Ekman DR, Ankley GT, Blazer VS, Collette TW, Reyero NG, Iwanowicz LR, Jorgenson ZG, Lee KE, Mazik PM, Miller DH, Perkins EJ, Smith ET, Tietge JE, Villeneuve DL (2013) Environmental reviews and case studies: biological effects-based tools for monitoring impacted surface waters in the Great Lakes: a multiagency program in support of the Great Lakes Restoration Initiative. Env Pract 409-426:409–426. https://doi.org/10.1017/S1466046613000458
Article Google Scholar
Embry MR, Belanger SE, Braunbeck TA, Galay-Burgos M, Halder M, Hinton DE, Léonard MA, Lillicrap A, Norberg-King T, Whale G (2010) The fish embryo toxicity test as an animal alternative method in hazard and risk assessment and scientific research. Aquat Toxicol 97(2):79–87. https://doi.org/10.1016/j.aquatox.2009.12.008
CAS Article Google Scholar
Escher BI, van Daele C, Dutt M, Tang JYM, Altenburger R (2013) Most oxidative stress response in water samples comes from unknown chemicals: the need for effect-based water quality trigger values. Env Sci Technol 47:7002–7011. https://doi.org/10.1021/es304793h
CAS Article Google Scholar
Esteban S, Gorga M, Petrovic M, González-Alonso M, Barceló D, Valcárcel Y (2014) Analysis and occurrence of endocrine-disrupting compounds and estrogenic activity in the surface waters of Central Spain. Sci. Tot. Environ. 466–467:939–951. https://doi.org/10.1016/j.scitotenv.2013.07.101
CAS Article Google Scholar
European Commission. Directive 2010/63/EU of the European Parliament and of the Council (2010) Official Journal (OJ L 276). http://data.europa.eu/eli/dir/2010/63/oj
Frena M, Bataglion GA, Tonietto AE, Eberlin MN, Alexandre MR, Madureira LAS (2016) Assessment of anthropogenic contamination with sterol markers in surface sediments of a tropical estuary (Itajaí-Açu, Brazil). Sci Tot Environ 544:432–438. https://doi.org/10.1016/j.scitotenv.2015.11.137
CAS Article Google Scholar
Gandar A, Laffaille P, Marty-Gasset N, Viala D, Molette C, Jean S (2017) Proteome response of fish under multiple stress exposure: effects of pesticide mixtures and temperature increase. Aquat Toxicol 184:61–77. https://doi.org/10.1016/j.aquatox.2017.01.004
CAS Article Google Scholar
Gavrilescu M, Demnerová K, Aamand J, Agathos S, Fava F (2015) Emerging pollutants in the environment: present and future challenges in biomonitoring, ecological risks and bioremediation. New Biotechnol 32(1):147–156. https://doi.org/10.1016/j.nbt.2014.01.001
CAS Article Google Scholar
Guo J, Iwata H (2017) Risk assessment of triclosan in the global environment using a probabilistic approach. Ecotox Environ Safe 143:111–119. https://doi.org/10.1016/j.ecoenv.2017.05.020
CAS Article Google Scholar
Gyimah E, Xu H, Dong X, Qiu X, Zhang Z, Bu Y, Akoto O (2021) Developmental neurotoxicity of low concentrations of bisphenol A and S exposure in zebrafish. Chemosphere 262:128045. https://doi.org/10.1016/j.chemosphere.2020.128045
CAS Article Google Scholar
Heo J, Kim S, Her N, Park CM, Yu M, Yoon Y (2019) Chapter 5 – removal of contaminants of emerging concern by FO, RO, and UF membranes in water and wastewater, Editor(s): Arturo J. Hernández-Maldonado, Lee Blaney, Contaminants of emerging concern in water and wastewater, Butterworth-Heinemann, 139-176, ISBN 9780128135617, https://doi.org/10.1016/B978-0-12-813561-7.00005-5
Hernández-Maldonado AJ, Blaney L (2019) Contaminants of emerging concern in water and wastewater: advanced treatment processes. https://doi.org/10.1016/C2016-0-05074-X
Huang GY, Liu YS, Liang YQ, Shi WJ, Hu LX, Tian F, Chen J, Ying GG (2016) Multi-biomarker responses as indication of contaminant effects in Gambusia affinis from impacted rivers by municipal effluents. Sci. Tot. Environ. 563–564:273–281. https://doi.org/10.1016/j.scitotenv.2016.04.127
CAS Article Google Scholar
Huang GY, Shi WJ, Fang GZ, Liang YQ, Liu YS, Liu YS, Hu LX, Chen HX, Xie L, Ying GG (2020) Endocrine disruption in western mosquitofish from open and closed aquatic ecosystems polluted by swine farm wastewaters. Environ Int 137:105552. https://doi.org/10.1016/j.envint.2020.105552
CAS Article Google Scholar
Jardim WF, Montagner CC, Pescara IC, Umbuzeiro GA, Bergamasco AM DD, Eldridge ML, Sodré FF (2012) An integrated approach to evaluate emerging contaminants in drinking water. Sep. Pur Technol. 84:3-8.https://doi.org/10.1016/j.seppur.2011.06.020
Jiang J, Chen Y, Yu R, Zhao X, Wang Q, Cai L (2016) Pretilachlor has the potential to induce endocrine disruption, oxidative stress, apoptosis and immunotoxicity during zebrafish embryo development. Environ Toxicol Pharmacol 42:125–134. https://doi.org/10.1016/j.etap.2016.01.006
CAS Article Google Scholar
Kao CM, Ou WJ, Lin HD, Eva AW, Wang TL, Chen SC (2019) Toxicity of diuron in HepG2 cells and zebrafish embryos. Ecotox Environ Safe. 172:432–438. https://doi.org/10.1016/j.ecoenv.2019.01.036
CAS Article Google Scholar
Keating KI (1985) A system of defined (sensu stricto) media for daphnid (Cladocera) culture. Water Res 19(1):73–78
CAS Article Google Scholar
Kim S, Lee S, Kim C, Liu X, Seo J, Jung H, Ji H, Hong S, Park J, Khim JS, Yoon S, Lee W, Park J, Choi K (2014) In vitro and in vivo toxicities of sediment and surface water in an area near a major steel industry of Korea: endocrine disruption, reproduction, or survival effects combined with instrumental analysis. Sci Tot Environ 470–471:1509–1516. https://doi.org/10.1016/j.scitotenv.2013.08.010
CAS Article Google Scholar
Kolpin DW, Skopec M, Meyer MT, Furlong ET, Zaugg SD (2004) Urban contribution of pharmaceuticals and other organic wastewater contaminants to streams during differing flow conditions. Sci Tot Environ 328(1–3):119–130. https://doi.org/10.1016/j.scitotenv.2004.01.015
CAS Article Google Scholar
Kovács R, Bakos K, Urbányi KJ, Gazsi G, Csepeli A, Appl AJ, Bencsik D, Csenki Z, Horváth A (2016) Acute and sub-chronic toxicity of four cytostatic drugs in zebrafish. Environ Sci Pollut Res 23:14718–14729. https://doi.org/10.1007/s11356-015-5036-z
CAS Article Google Scholar
Kurobe T, Lehman PW, Haque ME, Sedda T, Lesmeister S, The S (2018) Evaluation of water quality during successive severe drought years within Microcystis blooms using fish embryo toxicity tests for the San Francisco Estuary, California. Sci Tot Environ 610–611:1029–1037. https://doi.org/10.1016/j.scitotenv.2017.07.267
CAS Article Google Scholar
Lammer E, Kamp HG, Hisgen V, Koch M, Reinhard D, Salinas ER, Wendler K, Zok S, Braunbeck T (2009) Development of a flow-through system for the fish embryo toxicity test (FET) with the zebrafish (Danio rerio). Toxicol in Vitro 23(7):1436–1442. https://doi.org/10.1016/j.tiv.2009.05.014
CAS Article Google Scholar
Li S, He B, Wang J, Liu J, Hu X (2020) Risks of caffeine residues in the environment: necessity for a targeted ecopharmacovigilance program. Chemosphere. 243:125–343. https://doi.org/10.1016/j.chemosphere.2019.125343
CAS Article Google Scholar
López-Doval JC, Montagner CC, Alburquerque AF, Carlos VM, Umbuzeiro G, Pompêo M (2017) Nutrients, emerging pollutants and pesticides in a tropical urban reservoir: spatial distributions and risk assessment. Sci Tot Environ 575:1307–1324. https://doi.org/10.1016/j.scitotenv.2016.09.210
CAS Article Google Scholar
Machado KC, Grassi MT, Vidal C, Pescara IC, Jardim WF, Fernandes AN, Sodré FF, Almeida FV, Santana JS, Canela MC, Nunes CRO, Bichinho KM, Severo FJR (2016) A preliminary nationwide survey of the presence of emerging contaminants in drinking and source waters in Brazil. Sci. Tot. Environ. 572:138–146. https://doi.org/10.1016/j.scitotenv.2016.07.210
CAS Article Google Scholar
Meffe R, Bustamante I (2014) Emerging organic contaminants in surface water and groundwater: a first overview of the situation in Italy. Sci Tot Environ 481:280–295. https://doi.org/10.1016/j.scitotenv.2014.02.053
CAS Article Google Scholar
Meftaul IM, Venkateswarlu K, Dharmarajan R, Annamalai P, Megharaj M (2020) Pesticides in the urban environment: a potential threat that knocks at the door. Sci. Tot. Environ. 711:134612. https://doi.org/10.1016/j.scitotenv.2019.134612
CAS Article Google Scholar
Miller JN, Miller JC (2005) Statistics and chemometrics for analytical chemistry. Pearson Ed. 285pp
Montagner CC, Umbuzeiro GA, Pasquini C, Jardim WF (2014) Caffeine as an indicator of estrogenic activity in source water. Environ Sci Process Impacts 16:1866–1869. https://doi.org/10.1039/c4em00058g
CAS Article Google Scholar
Montagner CC, Sodré FF, Acayaba RD, Vidal C, Campestrini I, Locatelli MA, Pescara IC, Albuquerque AF, Umbuzeiro GA, Jardim WF (2019) Ten years-snapshot of the occurrence of emerging contaminants in drinking, surface and ground waters and wastewaters from São Paulo state, Brazil. J Braz Chem Soc. 30:614–632. https://doi.org/10.21577/0103-5053.20180232
CAS Article Google Scholar
Nascimento MTL, Santos ADO, Felix LC, Gomes G, Sá MO, Cunha DL, Vieira N, Hauser-DavisRA NJAB, Bila DM (2018) Determination of water quality, toxicity and estrogenic activity in a nearshore marine environment in Rio de Janeiro, Southeastern Brazil. Ecotox Environ Safe 149:197–202. https://doi.org/10.1016/j.ecoenv.2017.11.045
CAS Article Google Scholar
Neale PA, Ait-Aissa S, Brack W, Creusot N, Denison MS, Deutschmann B, Hilscherová K, Hollert H, Krauss M, Novák J (2015) Linking in vitro effects and detected organic micropollutants in surface water using mixture-toxicity modeling. Environ Sci Technol 49(24):14614–14624. https://doi.org/10.1021/acs.est.5b04083
CAS Article Google Scholar
Nilsen E, Smalling KL, Ahrens L, Gros M, Miglioranza KSB, Schoenfuss HL (2019) Critical review: grand challenges in assessing the adverse effects of contaminants of emerging concern on aquatic food webs. Environ Toxicol Chem 38(1):46–60. https://doi.org/10.1002/etc.4290
OECD (2013) Test No. 236: Fish Eembryo Acute Toxicity (FET) test, OECD guidelines for the testing of chemicals, section 2, OECD Publishing, Paris, https://doi.org/10.1787/9789264203709-en
Oliveira R, Domingues I, Grisolia CK, Soares AMVM (2009) Effects of triclosan on zebrafish early-life stages and adults. Environ Sci Pollut Res 16:679–688. https://doi.org/10.1007/s11356-009-0119-3
CAS Article Google Scholar
Oviedo KN, Aga DS (2016) Lessons learned from more than two decades of research on emerging contaminants in the environment. J Hazard Mater 316:242–251. https://doi.org/10.1016/j.jhazmat.2016.04.058
CAS Article Google Scholar
Pereira CDS, Maranho LA, Cortez FS, Pusceddu FH, Santos AR, Ribeiro DA, Cesar A, Guimarães LL (2016) Occurrence of pharmaceuticals and cocaine in a Brazilian coastal zone. Sci Tot Environ. 548–549:148–154. https://doi.org/10.1016/j.scitotenv.2016.01.051
CAS Article Google Scholar
Petersen K, Fetter E, Kah O, Brion F, Scholz S, Tollefsen KE (2013) Transgenic (cyp19a1b-GFP) zebrafish embryos as a tool for assessing combined effects of oestrogenic chemicals. Aquat Toxicol 138–139:88–97. https://doi.org/10.1016/j.aquatox.2013.05.001
CAS Article Google Scholar
Petrovic M, Eljarrat E, de Alda MJL, Barceló D (2002) Recent advances in the mass spectrometric analysis related to endocrine disrupting compounds in aquatic environmental samples. J Chromat A 974(1–2):23–51. https://doi.org/10.1016/S0021-9673(02)00907-X
CAS Article Google Scholar
Pintado-Herrera MG, González-Mazo E, Lara-Martín PA (2014) Determining the distribution of triclosan and methyl triclosan in estuarine settings. Chemosphere. 95:478–485. https://doi.org/10.1016/j.chemosphere.2013.09.101
CAS Article Google Scholar
Priac A, Morin-Crini N, Druart C, Gavoille S, Bradu C, Lagarrigue C, Torri G, Winterton P, Crini G (2017) Alkylphenol and alkylphenol polyethoxylates in water and wastewater: a review of options for their elimination. Arab J Chem 10(2):S3749–S3773. https://doi.org/10.1016/j.arabjc.2014.05.011
CAS Article Google Scholar
Pruvot B, Quiroz Y, Voncken A, Jeanray N, Piot A, Martial JA, Muller M (2012) A panel of biological tests reveals developmental effects of pharmaceutical pollutants on late stage zebrafish embryos. Reprod Toxicol 34(4):568–583. https://doi.org/10.1016/j.reprotox.2012.07.010
CAS Article Google Scholar
Pullaguri N, Nema S, Bhargava Y, Bhargava A (2020) Triclosan alters adult zebrafish behavior and targets acetylcholinesterase activity and expression. Environ Toxicol Pharm 75:103311. https://doi.org/10.1016/j.etap.2019.103311
CAS Article Google Scholar
Qian L, Liu J, Lin Z, Chen X, Yuan L, Shen G, Yang W, Wang D, Huang Y, Pang S, Mu C, Wang C, Li Y (2020) Evaluation of the spinal effects of phthalates in a zebrafish embryo assay. Chemosphere. 249:126144. https://doi.org/10.1016/j.chemosphere.2020.126144
CAS Article Google Scholar
Rah YC, Yoo MH, ChoiJ PS, Park HC, Oh KH, Lee SH, Kwon SY (2017) In vivo assessment of hair cell damage and developmental toxicity caused by gestational caffeine exposure using zebrafish (Danio rerio) models. NeurotoxicolTeratol. 64:1–7. https://doi.org/10.1016/j.ntt.2017.08.003
CAS Article Google Scholar
Rocha PS, Bernecker C, Strecker R, Mariani CF, Pompêo MLM, Storch V, Hollert H, Braunbeck T (2011) Sediment-contact fish embryo toxicity assay with Danio rerio to assess particle-bound pollutants in the Tiete River Basin (Sao Paulo, Brazil). Ecotoxicol Environ Saf 74(7):1951–1959. https://doi.org/10.1016/j.ecoenv.2011.07.009
CAS Article Google Scholar
Ryberg KR, Gilliom RJ (2015) Trends in pesticide concentrations and use for major rivers of the United States. Sci Total Environ 538:431–444. https://doi.org/10.1016/j.scitotenv.2015.06.095
CAS Article Google Scholar
Schmid S, Willi RA, Salgueiro-González N, Fent K (2020) Effects of new generation progestins, including as mixtures and in combination with other classes of steroid hormones, on zebrafish early life stages. Sci Tot Environ. 709:136262. https://doi.org/10.1016/j.scitotenv.2019.136262
CAS Article Google Scholar
Schmidt S, Busch W, Altenburger R, Küster E (2016) Mixture toxicity of water contaminants-effect analysis using the zebrafish embryo assay (Danio rerio). Chemosphere. 152:503–512. https://doi.org/10.1016/j.chemosphere.2016.03.006
CAS Article Google Scholar
Scholz S, Sela E, Blaha L, Braunbeck T, Galay-Burgos M, García-Franco M, Guinea J, Klüver G, Schirmer K, Tanneberger K, Tobor-Kapłon M, Witters H, Belanger S, Benfenati E, Creton S, Cronin MTD, Eggen RIL, Embry M, Ekman D, Gourmelon A, Halder M, Hardy B, Hartung T, Hubesch B, Jungmann D, Lampi MA, Lee L, Léonard M, Küster E, Lillicrap A, Luckenbach T, Murk AJ, Navas JM, Peijnenburg W, Repetto G, Salinas E, Schüürmann G, Spielmann H, Tollefsen KE, Walter-Rohde S, Whale G, Wheeler JR, Winter MJ (2013) A European perspective on alternatives to animal testing for environmental hazard identification and risk assessment. Reg Toxicol Pharm 67(3):506–530. https://doi.org/10.1016/j.yrtph.2013.10.003
Article Google Scholar
Schulte C, Nagel R (1994) Testing acute toxicity in embryo of Zebrafish, Brachydanio rerio as alternative to the acute fish test — preliminary results. ATLA 22:12–19. https://doi.org/10.1177/026119299402200104
Article Google Scholar
Schwarzenbach RP, Escher BI, Fenner K, Hofstetter TB, Johnson CA, Von Gunten U, Wehrli B (2006) The challenge of micropollutants in aquatic systems. Science 313(5790):1072–1077
CAS Article Google Scholar
Severo ES, Marins AT, Cerezer C, Costa D, Nunes M, Prestes OD, Zanella R, Loro VL (2020) Ecological risk of pesticide contamination in a Brazilian river located near a rural area: a study of biomarkers using zebrafish embryos. Ecotox Environ Safe 190:110071. https://doi.org/10.1016/j.ecoenv.2019.110071
CAS Article Google Scholar
Shen W, Lou B, Xu C, Yang G, Yu R, Wang X, Li X, Wang Q, Wang Y (2020) Lethal toxicity and gene expression changes in embryonic zebrafish upon exposure to individual and mixture of malathion, chlorpyrifos and lambda-cyhalothrin. Chemosphere. 239:124802. https://doi.org/10.1016/j.chemosphere.2019.124802
CAS Article Google Scholar
Silva MCG, Silva JF, Santos TP, Silva NPC, Santos AR, Andrade ALC, Souza EHLS, Cadena MRS, Sá FB, Silva Junior VA, Cadena PG (2019) The complexation of steroid hormones into cyclodextrin alters the toxic effects on the biological parameters of zebrafish (Danio rerio). Chemosphere. 214:330–340. https://doi.org/10.1016/j.chemosphere.2018.09.116
CAS Article Google Scholar
Smith KE, Schmidt SN, Dom N, Blust R, Holmstrup M, Mayer P (2013) Baseline toxic mixtures of non-toxic chemicals: “solubility addition” increases exposure for solid hydrophobic chemicals. Environ Sci Technol 47(4):2026–2033. https://doi.org/10.1021/es3040472
CAS Article Google Scholar
Sodré FF, Pescara IC, Montagner CC, Jardim WF (2010) Assessing selected estrogens and xenoestrogens in Brazilian surface waters by liquid chromatography–tandem mass spectrometry. Microchem J 96(1):92–98. https://doi.org/10.1016/j.microc.2010.02.012
CAS Article Google Scholar
Song M, Liang D, Liang Y, Chen M, Wang F, Wang H, Jiang G (2014) Assessing developmental toxicity and estrogenic activity of halogenated bisphenol A on zebrafish (Danio rerio). Chemosphere. 112:275–281. https://doi.org/10.1016/j.chemosphere.2014.04.084
CAS Article Google Scholar
Souza DB, Machado KS, Froehner S, ScapulatempoCF BT (2011) Distribution of n-alkanes in lacustrine sediments from subtropical lake in Brazil. Geochemistry. 71(2):171–176. https://doi.org/10.1016/j.chemer.2011.02.006
CAS Article Google Scholar
Souza RM, Seibert D, Quesada HB, Bassetti FJ, Fagundes-Klen MR, Bergamasco R (2020) Occurrence, impacts and general aspects of pesticides in surface water: a review. Process Saf Environ 135:22–37. https://doi.org/10.1016/j.psep.2019.12.035
CAS Article Google Scholar
Sposito JCV, Montagner CC, Casado M, Navarro-Martín L, Solórzano JCJ, Piña B, Grisolia AB (2018) Emerging contaminants in Brazilian rivers: occurrence and effects on gene expression in zebrafish (Danio rerio) embryos. Chemosphere. 209:696–704. https://doi.org/10.1016/j.chemosphere.2018.06.046
CAS Article Google Scholar
Starling MCVM, Amorim CC, Leão MMD (2019) Occurrence, control and fate of contaminants of emerging concern in environmental compartments in Brazil. J Hazard Mater 372:17–36. https://doi.org/10.1016/j.jhazmat.2018.04.043
CAS Article Google Scholar
Tse WKF, Yeung BHY, Wan HT, Wong CKC (2013) Early embryogenesis in zebrafish is affected by bisphenol A exposure. Biol. Open 2:466–471. https://doi.org/10.1242/bio.20134283
U.S. Geological Survey (USGS) (2017) Contaminants of emerging concern in the environment. Environmental Health - Toxic Substances Hydrology Program. https://toxics.usgs.gov/investigations/cec/index.php
Vale RL, Netto AM, Xavier BTL, Barreto MLP, Silva JPS (2019) Assessment of the gray water footprint of the pesticide mixture in a soil cultivated with sugarcane in the northern area of the State of Pernambuco, Brazil. J Clean Prod 234:925–932. https://doi.org/10.1016/j.jclepro.2019.06.282
CAS Article Google Scholar
van de Merwe JP, Neale PA, Melvin SD, Leusch FDL (2018) In vitro bioassays reveal that additives are significant contributors to the toxicity of commercial household pesticides. Aquatic Toxicol 199:263–268. https://doi.org/10.1016/j.aquatox.2018.03.033
CAS Article Google Scholar
Vieira DC, Noldin JA, Deschamps FC, Resgalla C (2016) Ecological risk analysis of pesticides used on irrigated rice crops in southern Brazil. Chemosphere. 162:48–54. https://doi.org/10.1016/j.chemosphere.2016.07.046
CAS Article Google Scholar
Vosges M, Kah O, Hinfray N, Chadili E, Le Page Y, Combarnous Y, Porcher JM, Brion F (2012) 17α-Ethinylestradiol and nonylphenol affect the development of forebrain GnRH neurons through an estrogen receptors-dependent pathway. Reprod Toxicol 33(2):198–204. https://doi.org/10.1016/j.reprotox.2011.04.005
CAS Article Google Scholar
Wagner SD, Kurobe T, Hammock BG, Lam CH, Wu G, Vasylieva N, Gee SJ, Hammock BD, The SJ (2017) Developmental effects of fipronil on Japanese medaka (Oryzias latipes) embryos. Chemosphere. 166:511–520. https://doi.org/10.1016/j.chemosphere.2016.09.069
CAS Article Google Scholar
Walter H, Consolaro F, Gramatica P, Scholze M, Altenburger R (2002) Mixture toxicity of priority pollutants at no observed effect concentrations (NOECs). Ecotoxicol. 11:299–310. https://doi.org/10.1023/A:1020592802989
CAS Article Google Scholar
Wang Q, Chen M, Shan G, Chen P, Cui S, Yi S, Zhu L (2017) Bioaccumulation and biomagnification of emerging bisphenol analogues in aquatic organisms from Taihu Lake, China. Sci Tot Environ 598:814–820. https://doi.org/10.1016/j.scitotenv.2017.04.167
CAS Article Google Scholar
Weber AA, Moreira DP, Melo RMC, Vieira ABC, Prado PS, Silva MAN, Bazzoli N, Rizzo E (2017) Reproductive effects of oestrogenic endocrine disrupting chemicals in Astyanax rivularis inhabiting headwaters of the Velhas River, Brazil. Sci Tot Environ 592:693–703. https://doi.org/10.1016/j.scitotenv.2017.02.181
CAS Article Google Scholar
Wirbisky SE, Weber GJ, Schlotman KE, Sepúlveda MS, Freeman JL (2016) Embryonic atrazine exposure alters zebrafish and human miRNAs associated with angiogenesis, cancer, and neurodevelopment. Food Chem Toxicol 98(Part A):25–33. https://doi.org/10.1016/j.fct.2016.03.027
CAS Article Google Scholar
Xia J, Niu C, Pei X (2010) Effects of chronic exposure to nonylphenol on locomotor activity and social behavior in zebrafish (Danio rerio). J Environ Sci. 22 (9)1435–1440. https://doi.org/10.1016/S1001-0742(09)60272-2
Xie H, Wang X, Chen J, Li X, Jia G, Zou Y, Zhang Y, Cui Y (2019) Occurrence, distribution and ecological risks of antibiotics and pesticides in coastal waters around Liaodong Peninsula, China. Sci Tot Environ. 656:946–951. https://doi.org/10.1016/j.scitotenv.2018.11.449
CAS Article Google Scholar
Xu M, Huang H, Li N, Li F, Wang D, Luo Q (2019) Occurrence and ecological risk of pharmaceuticals and personal care products (PPCPs) and pesticides in typical surface watersheds, China. Ecotoxicology and Environmental Safety 175:289–298. https://doi.org/10.1016/j.ecoenv.2019.01.131
CAS Article Google Scholar
Zhao JL, Ying GG, Wang L, Yang JF, Yang XB, Yang LH, Li X (2009) Determination of phenolic endocrine disrupting chemicals and acidic pharmaceuticals in surface water of the Pearl Rivers in South China by gas chromatography–negative chemical ionization–mass spectrometry. Sci Tot Environ. 407(2):962–974. https://doi.org/10.1016/j.scitotenv.2008.09.048
CAS Article Google Scholar
Zhao JL, Zhang QQ, Chen F, Wang L, Ying GG, Liu YS, Yang B, Zhou LJ, Liu S, Su HC, Zhang RQ (2013) Evaluation of triclosan and triclocarban at river basin scale using monitoring and modeling tools: implications for controlling of urban domestic sewage discharge. Water Res 47(1):395–405. https://doi.org/10.1016/j.watres.2012.10.022
CAS Article Google Scholar
Zhou S, Chen Q, Di Paolo C, Shao Y, Hollert H, Seiler TB (2019) Behavioral profile alterations in zebrafish larvae exposed to environmentally relevant concentrations of eight priority pharmaceuticals. Sci Total Environ 664:89–98. https://doi.org/10.1016/j.scitotenv.2019.01.300
CAS Article Google Scholar
Zoupa M, Zwart EP, Gremmer ER, Nugraha A, Compeer S, Slob W, van der Ven LTM (2020) Dose addition in chemical mixtures inducing craniofacial malformations in zebrafish (Danio rerio) embryos. Food Chem Toxicol 137:111117. https://doi.org/10.1016/j.fct.2020.111117
CAS Article Google Scholar

Download references

Acknowledgments

The authors thank Brazilian Council for Scientific and Technological Development (CNPq) for the financial support by doctorate scholarship (process number 141973/2014-5) and to the National Institute of Advanced Analytical Sciences and Technologies (INCTAA, CNPq Grant No. 465768/2014-8 and FAPESP Grant No. 2014/50951-4). The authors also thank the Environmental Agency of São Paulo state (CETESB) for the infrastructure, and scientific and technical support and Raphael D’Anna Acayaba for support in chemical analysis.

Funding

This study was financially supported by the National Institute of Advanced Analytical Sciences and Technologies (INCTAA, CNPq Grant No. 465768/2014-8 and FAPESP Grant No. 2014/50951-4) and National Council for Scientific and Technological Development (CNPq, Grant No. 141973/2014-5).

Author information

Affiliations

Centro de Química e Meio Ambiente, Instituto de Pesquisas Energéticas e Nucleares, São Paulo, Brazil
Gisela de Assis Martini, Sizue Ota Rogero & José Roberto Rogero
Instituto de Química, Universidade Estadual de Campinas, São Paulo, Brazil
Cassiana Carolina Montagner & Nívea Cristina Guedes Munin
Companhia Ambiental do Estado de São Paulo, São Paulo, Brazil
William Viveiros, Gilson Alves Quinaglia & Daniela Dayrell França
Laboratório Especial de Toxinologia Aplicada, Instituto Butantan, São Paulo, Brazil
Mônica Lopes-Ferreira
Universidade Federal do Amazonas, Manaus, Brazil
Nívea Cristina Guedes Munin

Authors

Gisela de Assis Martini
View author publications
You can also search for this author in PubMed Google Scholar
Cassiana Carolina Montagner
View author publications
You can also search for this author in PubMed Google Scholar
William Viveiros
View author publications
You can also search for this author in PubMed Google Scholar
Gilson Alves Quinaglia
View author publications
You can also search for this author in PubMed Google Scholar
Daniela Dayrell França
View author publications
You can also search for this author in PubMed Google Scholar
Nívea Cristina Guedes Munin
View author publications
You can also search for this author in PubMed Google Scholar
Mônica Lopes-Ferreira
View author publications
You can also search for this author in PubMed Google Scholar
Sizue Ota Rogero
View author publications
You can also search for this author in PubMed Google Scholar
José Roberto Rogero
View author publications
You can also search for this author in PubMed Google Scholar

Contributions

I declare that all the authors of this manuscript contributed to the methodological and theoretical development of this study. The sample collection and preparation were carried out by Gisela de Assis Martini, Gilson Alves Quináglia and Daniela Dayrell França; chemical analysis was carried out by Cassiana Carolina Montagner and Nívea Cristina Guedes Munin; the biological tests with zebrafish embryos were carried out by Gisela de Assis Martini, William Viveiros, and Mônica Lopes-Ferreira; José Roberto Rogero, Sizue Ota Rogero, and Cassiana Carolina Montagner contributed to the manuscript structure and development. The present version of the manuscript was written by Gisela de Assis Martini, as well as the statistical analysis. Lastly, it is true that all authors have read and approved the submitted version of this manuscript.

Corresponding author

Correspondence to Gisela de Assis Martini.

Ethics declarations

Ethics approval and consent to participate

Ethical Committee for Animals from Nuclear Energy Research Institute (CEUA/IPEN) registered under number 207/18 and obtained in February 15th 2018.

Consent for publication

Not applicable to this manuscript.

Competing interests

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Responsible Editor: Cinta Porte

Supplementary information

Table S1

(DOC 83 kb)

Table S2

(XLSX 35 kb)

Table S3

(XLSX 37 kb)

Table S4

(XLSX 152 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Martini, G.d., Montagner, C.C., Viveiros, W. et al. Emerging contaminant occurrence and toxic effects on zebrafish embryos to assess the adverse effects caused by mixtures of substances in the environment. Environ Sci Pollut Res 28, 20313–20329 (2021). https://doi.org/10.1007/s11356-020-11963-x

Download citation

Received: 28 September 2020
Accepted: 02 December 2020
Published: 06 January 2021
Issue Date: April 2021
DOI: https://doi.org/10.1007/s11356-020-11963-x

Keywords

Surface water
Contaminants of emerging concern
Chemical analysis
FET
Danio rerio embryos