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.
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Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.
References
Almond KM, Trombetta LD (2016) The effects of copper pyrithione, an antifouling agent, on developing zebrafish embryos. Ecotoxicology 25:389–398. https://doi.org/10.1007/s10646-015-1597-3
Almond KM, Trombetta LD (2017) Copper pyrithione, a booster biocide, induces abnormal muscle and notochord architecture in zebrafish embryogenesis. Ecotoxicology 26:855–867. https://doi.org/10.1007/s10646-017-1816-1
Alzieu C (2000) Impact of tributyltin on marine invertebrates. Ecotoxicology 9:71–76. https://doi.org/10.1023/A:1008968229409
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 (2016) Liver alterations in Oreochromis niloticus (Pisces) induced by insecticide imidacloprid: Histopathology and heat shock protein in situ localization. J Environ Sci Health B 51(12):881–887. https://doi.org/10.1080/03601234.2016.1240559
Arslan P, Ozeren SC (2021) A case study of 38 micro-organic pollutants contamination in Kirmir Stream, Turkey. Environ Qual Manag 10:20. https://doi.org/10.1002/tqem.21811
Arslan P, Özeren SC, Yurdakök Dikmen B (2021) The effects of endocrine disruptors on fish. Environ Res Technol 4(2):145–151. https://doi.org/10.35208/ert.860440
Bellas J, Granmo K, Beiras R (2005) Embryotoxicity of the antifouling biocide zinc pyrithione to sea urchin (Paracentrotus lividus) and mussel (Mytilus edulis). Mar Pollut Bull 50(11):1382–1385. https://doi.org/10.1016/j.marpolbul.2005.06.010
Bernet D, Schmidt H, Meier W, Burkhardt-Holm P, Wahli T (1999) Histopathology in fish: proposal for a protocol to access aquatic pollution. J Fish Dis 22(1):25–34
Bian X, Gao Y (2021) DNA methylation and gene expression alterations in zebrafish embryos exposed to cadmium. Environ Sci Pollut Res 28:30101–30110. https://doi.org/10.1007/s11356-021-12691-6
Blanchard J, Grosell M (2005) Effects of salinity on copper accumulation in the common killifish (Fundulus heteroclitus). Environ Toxicol Chem 24:1403–1413
Bones J, Thomas KV, Paull B (2006) 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 1132(1–2):157–164. https://doi.org/10.1016/j.chroma.2006.07.068
Castro İB, Machado FB, de Sousa GT, Paz-Villarraga C, Fillmann G (2021) How protected are marine protected areas: a case study of tributyltin in Latin America. J Environ Manage 278(2):111543. https://doi.org/10.1016/j.jenvman.2020.111543
Cengiz Eİ (2006) Gill and kidney histopathology in the freshwater fish Cyprinus carpio after acute exposure to deltamethrin. Environ Toxicol Pharmacol 22(2):200–204. https://doi.org/10.1016/j.etap.2006.03.006
Davidson AJ (2014) Kidney regeneration in fish. Nephron Exp Nephrol 126:45–49. https://doi.org/10.1159/000360660
Eriksson Wiklund AK, Börjesson T, Wiklund SJ (2006) Avoidance response of sediment living amphopods to zinc pyrithione as a measure of sediment toxicity. Mar Pollut Bull 52:96–99
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 (2020) Osmoregulatory profiles and gill histological changes in Nile tilapia (Oreochromis niloticus) exposed to lambda-cyhalothrin. Aquat Toxicol 227:105612. https://doi.org/10.1016/j.aquatox.2020.105612
Flammarion P, Brion F, Babut M, Garric J, Migeon B, Noury P, Thybaud E, Palazzi X, Tyler CR (2000) Induction of fish vitellogenin and alterations in testicular structure: preliminary results of estrogenic effects in chub (Leuciscus cephalus). Ecotoxicology 9:127–135. https://doi.org/10.1023/A:1008984616206
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 28(1):603–611. https://doi.org/10.1016/j.sjbs.2020.10.049
Guardiola FA, Cuesta A, Meseguer J, Esteban MA (2012) Risks of using antifouling biocides in aquaculture. Int J Mol Sci 13(2):1541–1560. https://doi.org/10.3390/ijms13021541
Günal AÇ, Erkmen B, Paçal E, Arslan P, Yıldırım Z, Erkoç F (2020) Sub-lethal effects of imidacloprid on Nile Tilapia (Oreochromis niloticus). Water Air Soil Pollut 231:4. https://doi.org/10.1007/s11270-019-4366-8
Günal AÇ, Tunca SK, Arslan P, Gül G, Sepici Dinçel A (2021) How does sublethal permethrin effect non-target aquatic organisms? Environ Sci Pollut Res 28:52405–52417. https://doi.org/10.1007/s11356-021-14475-4
Haque MN, Nam SE, Eom HJ, Kim SK, Rhee JS (2020) 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 156:111276. https://doi.org/10.1016/j.marpolbul.2020.111276
Hedayati A (2016) Liver as a target organ for eco-toxicological studies. J Coast Zone Manag 19:e118. https://doi.org/10.4172/2473-3350.1000e118
Imai S, Koyama J, Fujii K (2005) Effects of 17β-estradiol on the reproduction of Java-medaka (Oryzias javanicus), a new test fish species. Mar Pollut Bull 51(8–12):708–714. https://doi.org/10.1016/j.marpolbul.2005.02.018
Karatas T, Yildirim S, Arslan H, Aggul AG (2019) The effects on brown trout (Salmo trutta fario) of different concentrations of deltamethrin. Comp Biochem Physiol Part C: Toxicol Pharmacol 226:108606. https://doi.org/10.1016/j.cbpc.2019.108606
Katranitsas A, Castritsi-Catharios J, Persoone G (2003) The effects of a copper-based antifouling paint on mortality and enzymatic activity of a non-target marine organism. Mar Pollut Bull 46:1491–1494
Lun LG (1968) Manual of histological staining methods of the armed forces institute of pathology, 3rd edn. McGraw-Hill Book Company, New York, p 258
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.
Mahboob S, Al-Ghanim KA, Al-Balawi HF, Al-Misned F, Ahmed Z (2020) Toxicological effects of heavy metals on histological alterations in various organs in Nile tilapia (Oreochromis niloticus) from freshwater reservoir. J King Saud Univ Sci 32(1):970–973. https://doi.org/10.1016/j.jksus.2019.07.004
Maraldo K, Dahllöf I (2004) Indirect estimation of degradation time for zinc pyrithione and copper pyrithione in seawater. Mar Pollut Bull 48(9–10):894–901. https://doi.org/10.1016/j.marpolbul.2003.11.013
Marcheselli M, Rustichelli C, Mauri M (2010) Novel antifouling agent zinc pyrithione: determination, acute toxicity, and bioaccumulation in marine mussels (Mytilus galloprovincialis). Environ Toxicol Chem 29(11):2583–2592. https://doi.org/10.1002/etc.316 (PMID: 20853456)
McIntyre JK, Baldwin DH, Meador JP, Scholz NL (2008) Chemosensory deprivation in juvenile Coho salmon exposed to dissolved copper under varying water chemistry conditions. Environ Sci Technol 42:1352–1358
Mirghaed AT, Ghelicgpour M, Mirzargar SS, Joshaghani H, Mousavi HE (2018) Toxic effects of indoxacarb on gill and kidney histopathology and biochemical indicators in common carp (Cyprinus carpio). Aquac Res 49(4):1616–1627. https://doi.org/10.1111/are.13617
Mishra AK, Mohanty B (2008) 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 26(2):136–141. https://doi.org/10.1016/j.etap.2008.02.010
Mochida K, Ito K, Harino H, Kakuno A, Fujii K (2006) 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 25(11):3058–3064
Mohamat-Yusuff F, Sarah-Nabila AG, Zulkifli SZ, Azmai MNA, Ibrahim WNW, Yusof S, Ismail A (2018) Acute toxicity test of copper pyrithione on Javanese medaka and the behavioural stress symptoms. Mar Pollut Bull 127:150–153. https://doi.org/10.1016/j.marpolbul.2017.11.046
Noguleria AF, Pereira JL, Antunes SC, Gonçalves FJM, Nunes B (2018) Effects of zinc pyrithione on biochemical parameters of the freshwater Asian clam Corbicula fluminea. Aquat Toxicol 204:100–106. https://doi.org/10.1016/j.aquatox.2018.08.021
Nunes B, Costa M (2019) 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 26(13):13551–13559. https://doi.org/10.1007/s11356-019-04810-1
Nunes B, Braga MR, Campos JC, Gomes R, Ramos AS, Antunes SC, Correia AT (2015) Ecotoxicological effect of zinc pyrithione in the freshwater fish Gambusia holbrooki. Ecotoxicology 24(9):1896–1905. https://doi.org/10.1007/s10646-015-1525-6
Ohji M, Harino H, Langston W (2019) Differences in susceptibility of marine bacterial communities to metal pyrithiones, their degradation compounds and organotin antifouling biocides. J Mar Biolog Assoc 99(5):1033–1039. https://doi.org/10.1017/S0025315418001169
Okoumassoun L-E, Brochu C, Deblois C, Akponan S, Marion M, Averill-Bates D, Denizeau F (2002) Vitellogenin in tilapia male fishes exposed to organochlorine pesticides in Ouémé River in Republic of Benin. Sci Total Environ 299(1–3):163–172. https://doi.org/10.1016/S0048-9697(01)01053-1
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 (2021) Correlation between heavy metal-induced histopathological changes and trophic interactions between different fish species. Appl Sci 11:3760. https://doi.org/10.3390/app11093760
Presnell JK, Schreibman MP (1997) Humason’s animal tissue techniques. The John Hopkins University Press, Baltimore
Richmonds C, Dutta H (1989) Histopathological changes induced by malathion in the gills of bluegill Lepomis macrochirus. B Environ Contam Toxicol 43:123–130
Sánchez-Bayo F, Goka K (2005) Unexpected effects of zinc pyrithione and imidacloprid on Japanese medaka fish (Oryzias latipes). Aquat Toxicol 74:285–293. https://doi.org/10.1016/j.aquatox.2005.06.003
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
Sun J, Fang R, Wang H, Xu DX, Yang J, Huang X, Cozzolino D, Fang M, Huang Y (2022) A review of environmental metabolism disrupting chemicals and effect biomarkers associating disease risks: where exposomics meets metabolomics. Environ Int 158:106941. https://doi.org/10.1016/j.envint.2021.106941
Tian H, Ru S, Wang Z, Cai W, Wang W (2009) Estrogenic effects of monocrotophos evaluated by vitellogenin mRNA and protein induction in male goldfish (Carassius auratus). Comp Biochem Physiol Part C: Toxicol Pharmacol 150(2):231–236. https://doi.org/10.1016/j.cbpc.2009.04.014
Tresnakova N, Günal AÇ, Kankılıç GB, Paçal E, Tavşanoğlu ÜN, Uyar R, Erkoç F (2020) 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 36:292–308
Velmurugan B, Selvanayagam M, Cengiz Eİ, Unlu E (2007) The effects of fenvalerate on different tissues of freshwater fish Cirrhinus mrigala. J Environ Sci Health Part B 42(2):157–163. https://doi.org/10.1080/03601230601123292
Verma SK, Nandi A, Sinha A, Patel P, Jha E, Mohanty S, Panda PK, Ahuja R, Mishra YK, Suar M (2021) Zebrafish (Danio rerio) as an ecotoxicological model for nanomaterial induced toxicity profiling. Precis Nanomed 4(1):750–781
Viarengo A, Pertica M, Mancinelli G, Burlando B, Canesi L, Orunesu M (1996) In vivo effects of copper on calcium homeostasis mechanisms of mussel gill cell plasma membranes. Comp Biochem Physiol Part C 113:421–425
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
Yebra DM, Kiil S, Dam-Johansen K (2004) Antifouling technology-past, present and future steps towards efficient and environmentally friendly antifouling coatings. Prog Org Coat 50(2):75–104
Yoon KS, Youn N, Gu H, Kwack SJ (2017) Estrogenic activity of zinc pyrithione: an in vivo and in vitro study. Environ Health Toxicol 32:e2017004. https://doi.org/10.5620/eht.e2017004
Zezza D, Bisegna A, Angelozzi G, Merola C, Conte A, Amorena M, Perugini M (2020) Impact of endocrine disruptors on vitellogenin concentrations in Wild Brown Trout (Salmo trutta trutta). Bull Environ Contam Toxicol 105:218–223. https://doi.org/10.1007/s00128-020-02916-8
Zhao Y, Liu Y, Sun J, Sha H, Yang Y, Ye Q, Yang Q, Huang B, Yu Y, Huang H (2018) Acute toxic responses of embryo-larval zebrafish to zinc pyrithione (ZPT) reveal embryological and developmental toxicity. Chemosphere. https://doi.org/10.1016/j.chemosphere.2018.04.010
Zhao Y, Meng F, Ding C, Yu Y, Zhang G, Tzeng C (2020) Gender-differentiated metabolic abnormalities of adult zebrafish with zinc pyrithione (ZPT)-induced hepatotoxicity. Chemosphere 257:127177. https://doi.org/10.1016/j.chemosphere.2020.12
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This study was funded by Gazi University Science Research Projects (Grant Number 18/2017-02).
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AÇG and ASD designed the study. AÇG, Nİ, and RT performed the experiments. PA wrote the manuscript. AÇG, ASD, and PA revised the manuscript. All authors read and approved the manuscript.
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Günal, A.Ç., Arslan, P., İpiçürük, N. et al. Determination of endocrine disrupting effects of the antifouling pyrithiones on zebrafish (Danio rerio). Energ. Ecol. Environ. 7, 523–531 (2022). https://doi.org/10.1007/s40974-022-00245-6
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DOI: https://doi.org/10.1007/s40974-022-00245-6