Determination of endocrine disrupting effects of the antifouling pyrithiones on zebrafish (Danio rerio)

Aysel Çağlan Günal , Pınar Arslan , Nagehan İpiçürük , Rabia Tural , Aylin Sepici Dinçel

Energy, Ecology and Environment ›› 2022, Vol. 7 ›› Issue (5) : 523 -531.

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Energy, Ecology and Environment ›› 2022, Vol. 7 ›› Issue (5) : 523 -531. DOI: 10.1007/s40974-022-00245-6
Original Article

Determination of endocrine disrupting effects of the antifouling pyrithiones on zebrafish (Danio rerio)

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Abstract

Bacteria, algae, and fungi are the organisms affected by biocidal substances, which are widely used. Apart from these, they can also have toxic effects on various aquatic organisms. Copper pyrithione (CPT) and zinc pyrithione (ZPT) are used as an alternative to tributyltin, which is forbidden and known to be highly toxic to the aquatic ecosystem. However, there is lacking information about histopathological alterations and endocrine disrupting effects of these substances. Therefore, this study was aimed to investigate the effects of ZPT, CPT, and their mixtures on the histological changes in the tissues and on the vitellogenin hormone in male zebrafish. Substances caused hyperemia, epithelial lifting, telangiectasis, and hyperplasia in the gill tissue. In the liver tissue, hyperemia, hydropic degeneration and necrosis were observed. In addition, apoptosis was found in the gill, liver, and testicle of the tissues as a result of the TUNEL assay. Vitellogenin hormone, on the other hand, increased in the experimental groups compared to the control groups (p < 0.05). According to the obtained results, these substances, which are used as alternative antifouling materials, show as endocrine disrupting compounds by acting on vitellogenin as well as causing histopathological changes.

Keywords

Danio rerio / Zinc pyrithione / Copper pyrithione / Endocrine disruptors / Histological alterations / Vitellogenin

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Aysel Çağlan Günal, Pınar Arslan, Nagehan İpiçürük, Rabia Tural, Aylin Sepici Dinçel. Determination of endocrine disrupting effects of the antifouling pyrithiones on zebrafish (Danio rerio). Energy, Ecology and Environment, 2022, 7(5): 523-531 DOI:10.1007/s40974-022-00245-6

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References

[1]

Almond KM, Trombetta LD. The effects of copper pyrithione, an antifouling agent, on developing zebrafish embryos. Ecotoxicology, 2016, 25: 389-398

[2]

Almond KM, Trombetta LD. Copper pyrithione, a booster biocide, induces abnormal muscle and notochord architecture in zebrafish embryogenesis. Ecotoxicology, 2017, 26: 855-867

[3]

Alzieu C. Impact of tributyltin on marine invertebrates. Ecotoxicology, 2000, 9: 71-76

[4]

Ansoar-Rodríguez Y, Christofoletti CA, Correia JE, de Souza RB, Moreira-de-Sousa C, Marcato AC, Bueno OC, Malaspina O, Silva-Zacarin EC, Fontanetti CS. Liver alterations in Oreochromis niloticus (Pisces) induced by insecticide imidacloprid: Histopathology and heat shock protein in situ localization. J Environ Sci Health B, 2016, 51(12): 881-887

[5]

Arslan P, Ozeren SC. A case study of 38 micro-organic pollutants contamination in Kirmir Stream, Turkey. Environ Qual Manag, 2021, 10: 20

[6]

Arslan P, Özeren SC, Yurdakök Dikmen B. The effects of endocrine disruptors on fish. Environ Res Technol, 2021, 4(2): 145-151

[7]

Bellas J, Granmo K, Beiras R. Embryotoxicity of the antifouling biocide zinc pyrithione to sea urchin (Paracentrotus lividus) and mussel (Mytilus edulis). Mar Pollut Bull, 2005, 50(11): 1382-1385

[8]

Bernet D, Schmidt H, Meier W, Burkhardt-Holm P, Wahli T. Histopathology in fish: proposal for a protocol to access aquatic pollution. J Fish Dis, 1999, 22(1): 25-34

[9]

Bian X, Gao Y. DNA methylation and gene expression alterations in zebrafish embryos exposed to cadmium. Environ Sci Pollut Res, 2021, 28: 30101-30110

[10]

Blanchard J, Grosell M. Effects of salinity on copper accumulation in the common killifish (Fundulus heteroclitus). Environ Toxicol Chem, 2005, 24: 1403-1413

[11]

Bones J, Thomas KV, Paull B. Improved method for the determination of zinc pyrithione in environmental water samples incorporating on-line extraction and preconcentration coupled with liquid chromatography atmospheric pressure chemical ionisation mass spectrometry. J Chromatogr A, 2006, 1132(1–2): 157-164

[12]

Castro İB, Machado FB, de Sousa GT, Paz-Villarraga C, Fillmann G. How protected are marine protected areas: a case study of tributyltin in Latin America. J Environ Manage, 2021, 278 2

[13]

Cengiz . Gill and kidney histopathology in the freshwater fish Cyprinus carpio after acute exposure to deltamethrin. Environ Toxicol Pharmacol, 2006, 22(2): 200-204

[14]

Davidson AJ. Kidney regeneration in fish. Nephron Exp Nephrol, 2014, 126: 45-49

[15]

Eriksson Wiklund AK, Börjesson T, Wiklund SJ. Avoidance response of sediment living amphopods to zinc pyrithione as a measure of sediment toxicity. Mar Pollut Bull, 2006, 52: 96-99

[16]

Fernandes CE, da Silveira AW, do Nascimento Silva AL, de Souza AI, Povh JA, dos Santos Jaques JA, dos Anjos dos Santos E, Yonekawa MKA, de Barros Penteadoall B, Franco-Belussi L Osmoregulatory profiles and gill histological changes in Nile tilapia (Oreochromis niloticus) exposed to lambda-cyhalothrin. Aquat Toxicol, 2020, 227

[17]

Flammarion P, Brion F, Babut M, Garric J, Migeon B, Noury P, Thybaud E, Palazzi X, Tyler CR. Induction of fish vitellogenin and alterations in testicular structure: preliminary results of estrogenic effects in chub (Leuciscus cephalus). Ecotoxicology, 2000, 9: 127-135

[18]

Ghayyur S, Khan MF, Tabassum S, Ahmad MS, Sajid M, Badshah K, Khan MA, Saira SG, Khan NA, Ahmad B. Qamer S (2021) A comparative study on the effects of selected pesticides on hemato-biochemistry and tissue histology of freshwater fish Cirrhinus mrigala (Hamilton, 1822). Saudi J Biol Sci, 2021, 28(1): 603-611

[19]

Guardiola FA, Cuesta A, Meseguer J, Esteban MA. Risks of using antifouling biocides in aquaculture. Int J Mol Sci, 2012, 13(2): 1541-1560

[20]

Günal , Erkmen B, Paçal E, Arslan P, Yıldırım Z, Erkoç F. Sub-lethal effects of imidacloprid on Nile Tilapia (Oreochromis niloticus). Water Air Soil Pollut, 2020, 231: 4

[21]

Günal , Tunca SK, Arslan P, Gül G, Sepici Dinçel A. How does sublethal permethrin effect non-target aquatic organisms?. Environ Sci Pollut Res, 2021, 28: 52405-52417

[22]

Haque MN, Nam SE, Eom HJ, Kim SK, Rhee JS. Exposure to sublethal concentrations of zinc pyrithione inhibits growth and survival of marine polychaete through induction of oxidative stress and DNA damage. Mar Pollut Bull, 2020, 156

[23]

Hedayati A. Liver as a target organ for eco-toxicological studies. J Coast Zone Manag, 2016, 19

[24]

Imai S, Koyama J, Fujii K. Effects of 17β-estradiol on the reproduction of Java-medaka (Oryzias javanicus), a new test fish species. Mar Pollut Bull, 2005, 51(8–12): 708-714

[25]

Karatas T, Yildirim S, Arslan H, Aggul AG. The effects on brown trout (Salmo trutta fario) of different concentrations of deltamethrin. Comp Biochem Physiol Part C: Toxicol Pharmacol, 2019, 226

[26]

Katranitsas A, Castritsi-Catharios J, Persoone G. The effects of a copper-based antifouling paint on mortality and enzymatic activity of a non-target marine organism. Mar Pollut Bull, 2003, 46: 1491-1494

[27]

Lun LG. Manual of histological staining methods of the armed forces institute of pathology, 1968 3 New York McGraw-Hill Book Company 258

[28]

Magner J, Kaj L, Brorström-Lunden E (2013) Results from the Swedish National Screening Programme 2012, Subreport 4: Pyrithones. IVL Swedish Environmental Research Institute Ltd. Swedish Environmental Research Institute (IVL). IVL Report B2137.

[29]

Mahboob S, Al-Ghanim KA, Al-Balawi HF, Al-Misned F, Ahmed Z. Toxicological effects of heavy metals on histological alterations in various organs in Nile tilapia (Oreochromis niloticus) from freshwater reservoir. J King Saud Univ Sci, 2020, 32(1): 970-973

[30]

Maraldo K, Dahllöf I. Indirect estimation of degradation time for zinc pyrithione and copper pyrithione in seawater. Mar Pollut Bull, 2004, 48(9–10): 894-901

[31]

Marcheselli M, Rustichelli C, Mauri M. Novel antifouling agent zinc pyrithione: determination, acute toxicity, and bioaccumulation in marine mussels (Mytilus galloprovincialis). Environ Toxicol Chem, 2010, 29(11): 2583-2592 PMID: 20853456

[32]

McIntyre JK, Baldwin DH, Meador JP, Scholz NL. Chemosensory deprivation in juvenile Coho salmon exposed to dissolved copper under varying water chemistry conditions. Environ Sci Technol, 2008, 42: 1352-1358

[33]

Mirghaed AT, Ghelicgpour M, Mirzargar SS, Joshaghani H, Mousavi HE. Toxic effects of indoxacarb on gill and kidney histopathology and biochemical indicators in common carp (Cyprinus carpio). Aquac Res, 2018, 49(4): 1616-1627

[34]

Mishra AK, Mohanty B. Acute toxicity impacts of hexavalent chromium on behavior and histopathology of gill, kidney and liver of the freshwater fish, Channa punctatus (Bloch). Environ Toxicol Pharmacol, 2008, 26(2): 136-141

[35]

Mochida K, Ito K, Harino H, Kakuno A, Fujii K. Acute toxicity of pyrithione antifouling biocides and joint toxicity with copper to red sea bream (Pagrus major) and toy shrimp (Heptacarpus futilirostris). Environ Toxicol Chem, 2006, 25(11): 3058-3064

[36]

Mohamat-Yusuff F, Sarah-Nabila AG, Zulkifli SZ, Azmai MNA, Ibrahim WNW, Yusof S, Ismail A. Acute toxicity test of copper pyrithione on Javanese medaka and the behavioural stress symptoms. Mar Pollut Bull, 2018, 127: 150-153

[37]

Noguleria AF, Pereira JL, Antunes SC, Gonçalves FJM, Nunes B. Effects of zinc pyrithione on biochemical parameters of the freshwater Asian clam Corbicula fluminea. Aquat Toxicol, 2018, 204: 100-106

[38]

Nunes B, Costa M. Study of the effects of zinc pyrithione in biochemical parameters of the Polychaeta Hediste diversicolor: evidences of neurotoxicity at ecologically relevant concentrations. Environ Sci Pollut Res Int, 2019, 26(13): 13551-13559

[39]

Nunes B, Braga MR, Campos JC, Gomes R, Ramos AS, Antunes SC, Correia AT. Ecotoxicological effect of zinc pyrithione in the freshwater fish Gambusia holbrooki. Ecotoxicology, 2015, 24(9): 1896-1905

[40]

Ohji M, Harino H, Langston W. Differences in susceptibility of marine bacterial communities to metal pyrithiones, their degradation compounds and organotin antifouling biocides. J Mar Biolog Assoc, 2019, 99(5): 1033-1039

[41]

Okoumassoun L-E, Brochu C, Deblois C, Akponan S, Marion M, Averill-Bates D, Denizeau F. Vitellogenin in tilapia male fishes exposed to organochlorine pesticides in Ouémé River in Republic of Benin. Sci Total Environ, 2002, 299(1–3): 163-172

[42]

Onita B, Albu P, Herman H, Balta C, Lazar V, Fulop A, Baranyai E, Harangi S, Keki S, Nagy L, Nagy T, Jozsa V, Gal D, Györe K, Stan M, Hermenean A, Dinischiotu A. Correlation between heavy metal-induced histopathological changes and trophic interactions between different fish species. Appl Sci, 2021, 11: 3760

[43]

Presnell JK, Schreibman MP. Humason’s animal tissue techniques, 1997 Baltimore The John Hopkins University Press

[44]

Richmonds C, Dutta H. Histopathological changes induced by malathion in the gills of bluegill Lepomis macrochirus. B Environ Contam Toxicol, 1989, 43: 123-130

[45]

Sánchez-Bayo F, Goka K. Unexpected effects of zinc pyrithione and imidacloprid on Japanese medaka fish (Oryzias latipes). Aquat Toxicol, 2005, 74: 285-293

[46]

Standing Committee on Biocidal Products (2014) Regulation (EU) No 528/2012 concerning the making available on the market and use of biocidal products Evaluation of active substances Copper pyrithoione Product type 21. http://dissemination.echa.europa.eu/Biocides/ActiveSubstances/1275-21/1275-21_Assessment_Report.pdf

[47]

Sun J, Fang R, Wang H, Xu DX, Yang J, Huang X, Cozzolino D, Fang M, Huang Y. A review of environmental metabolism disrupting chemicals and effect biomarkers associating disease risks: where exposomics meets metabolomics. Environ Int, 2022, 158

[48]

Tian H, Ru S, Wang Z, Cai W, Wang W. Estrogenic effects of monocrotophos evaluated by vitellogenin mRNA and protein induction in male goldfish (Carassius auratus). Comp Biochem Physiol Part C: Toxicol Pharmacol, 2009, 150(2): 231-236

[49]

Tresnakova N, Günal , Kankılıç GB, Paçal E, Tavşanoğlu ÜN, Uyar R, Erkoç F. Sub-lethal toxicities of zinc pyrithione, copper pyrithione alone and in combination to the indicator mussel species Unio crassus Philipsson, 1788 (Bivalvia, Unionidae). Chem Ecol, 2020, 36: 292-308

[50]

Velmurugan B, Selvanayagam M, Cengiz , Unlu E. The effects of fenvalerate on different tissues of freshwater fish Cirrhinus mrigala. J Environ Sci Health Part B, 2007, 42(2): 157-163

[51]

Verma SK, Nandi A, Sinha A, Patel P, Jha E, Mohanty S, Panda PK, Ahuja R, Mishra YK, Suar M. Zebrafish (Danio rerio) as an ecotoxicological model for nanomaterial induced toxicity profiling. Precis Nanomed, 2021, 4(1): 750-781

[52]

Viarengo A, Pertica M, Mancinelli G, Burlando B, Canesi L, Orunesu M. In vivo effects of copper on calcium homeostasis mechanisms of mussel gill cell plasma membranes. Comp Biochem Physiol Part C, 1996, 113: 421-425

[53]

Woldegiorgis A, Remberger M, Kaj L, Green J, Ekheden Y, Palm-Cousins A, BrorströmLundén E, Dye C, Aspmo K, Vadset M, Schlabach M, Langford K (2007) Results from the Swedish National Screening Programme 2006. Subreport 3: Zinc pyritione and Irgarol 1051. Swedish Environmental Research Institute (IVL). IVL Report B1764

[54]

Yebra DM, Kiil S, Dam-Johansen K. Antifouling technology-past, present and future steps towards efficient and environmentally friendly antifouling coatings. Prog Org Coat, 2004, 50(2): 75-104

[55]

Yoon KS, Youn N, Gu H, Kwack SJ. Estrogenic activity of zinc pyrithione: an in vivo and in vitro study. Environ Health Toxicol, 2017, 32

[56]

Zezza D, Bisegna A, Angelozzi G, Merola C, Conte A, Amorena M, Perugini M. Impact of endocrine disruptors on vitellogenin concentrations in Wild Brown Trout (Salmo trutta trutta). Bull Environ Contam Toxicol, 2020, 105: 218-223

[57]

Zhao Y, Liu Y, Sun J, Sha H, Yang Y, Ye Q, Yang Q, Huang B, Yu Y, Huang H. Acute toxic responses of embryo-larval zebrafish to zinc pyrithione (ZPT) reveal embryological and developmental toxicity. Chemosphere, 2018

[58]

Zhao Y, Meng F, Ding C, Yu Y, Zhang G, Tzeng C. Gender-differentiated metabolic abnormalities of adult zebrafish with zinc pyrithione (ZPT)-induced hepatotoxicity. Chemosphere, 2020, 257

Funding

Gazi Üniversitesi(18/2017-02)

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