Biomarker-based assessment of sodium pyrithione toxicity in the freshwater mussel Unio sp.

Kevser Yılmaz; Feriha Yıldırım Ekim; Aysel Çağlan Günal; Belda Erkmen; Pınar Arslan Yüce; Zuhal Yıldırım; Figen Ünlü Erkoç

doi:10.55779/nsb18212875

Authors

Kevser Yılmaz Gazi University, Graduate School of Natural and Applied Sciences, Department of Environmental Sciences, Ankara (TR) https://orcid.org/0000-0001-6912-2696
Feriha Yıldırım Ekim Gazi University, Graduate School of Natural and Applied Sciences, Department of Environmental Sciences, Ankara (TR) https://orcid.org/0000-0003-4938-3922
Aysel Çağlan Günal 1) Gazi University, Graduate School of Natural and Applied Sciences, Department of Environmental Sciences, Ankara; 2) Gazi University, Gazi Education Faculty, Department of Biology Education, Ankara (TR) https://orcid.org/0000-0002-9072-543X
Belda Erkmen Aksaray University, Science and Letters Faculty, Department of Biology, Aksaray (TR) https://orcid.org/0000-0003-2841-0928
Pınar Arslan Yüce Çankırı Karatekin University, Faculty of Science, Department of Biology, Çankırı (TR) https://orcid.org/0000-0001-5910-2835
Zuhal Yıldırım Etimesgut Public Health Laboratory, Etimesgut, Ankara (TR) https://orcid.org/0000-0002-2808-7860
Figen Ünlü Erkoç 6 Başkent University, Faculty of Engineering, Department of Biomedical Engineering, Etimesgut, Ankara (TR) https://orcid.org/0000-0003-0658-2243

DOI:

https://doi.org/10.55779/nsb18212875

Keywords:

biocide, freshwater mussel, histopathology, oxidative stress biomarkers, sodium pyrithione, TUNEL

Abstract

Sodium pyrithione (NaPT) is widely used as a biocide in laundry detergents and anti-dandruff shampoos. The sublethal effects of NaPT on the freshwater mussel model organism Unio sp. were assessed using multiple biomarkers. A semi-static bioassay was established, and mussels were exposed to an environmentally relevant concentration of 5 μg L⁻¹ NaPT for 96 h. Total hemocyte counts did not differ significantly between the control (C) and experimental (E) groups, although the exposed group showed higher mean counts. Malondialdehyde (MDA), used as a lipid peroxidation biomarker, increased significantly in digestive gland (DG) tissues compared with controls (p<0.001), indicating lipid peroxidation. Gill (G) MDA levels also increased, but not significantly (p>0.05). GSH levels increased significantly in DG (p<0.05), whereas the increase in gill tissue was not significant (p>0.05). AOPP values in the digestive glands and gills of exposed mussels showed significant decreases compared with controls (p<0.05). SOD values decreased in DG but not significantly, whereas nonsignificant increases were recorded in G. The same trend was observed for GPx in DG, while G showed a slight decrease in GPx values. No histopathological alterations were observed in control tissues or in the gonads (ovary and testes), muscle, and mantle tissues of exposed mussels. Hydropic degeneration was observed in DG, and hyperplasia was detected in G. TUNEL analysis showed genotoxic damage, with intense apoptotic cells in DG and testes tissues compared with the control group, whereas no significant findings were observed in the gill and ovary tissues. These results indicate that sublethal NaPT exposure affects several tissues and antioxidant defence systems of freshwater Unio sp.

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References

Arslan P, Gül G, Günal AÇ (2023). How do biocidals affect the non-target marine organisms: the short-term effects of antifouling agent sodium pyrithione on Mediterranean mussels (Mytilus galloprovincialis, Lamark 1819). Environmental Science and Pollution Research, 30: 118332–118340. https://doi.org/10.1007/s11356-023-30611-8

Azizi G, Layachi M, Akodad M, Yáñez-Ruiz DR, Martín-García AI, Baghour M, et al. (2018). Seasonal variations of heavy metals content in mussels (Mytilus galloprovincialis) from Cala Iris offshore (Northern Morocco). Marine Pollution Bulletin, 137: 688–694. https://doi.org/10.1016/j.marpolbul.2018.06.052

Bat L, Oztekin A, Arıcı E, Sahin F (2021). Mytilus galloprovincialis and metal contaminants: health risk assessment from Sinop coasts. The Korean Journal of Food & Health Convergence, 7(4): 13–21.

Bradford MM (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72: 248–254. https://doi.org/10.1016/0003-2697(76)90527-3

Brand SJ, Erasmus JH, Labuschagne M, Grabner D, Nachev M, Zimmermann S, et al. (2019). Bioaccumulation and metal-associated biomarker responses in a freshwater mussel, Dreissena polymorpha, following short-term platinum exposure. Environmental Pollution, 246: 69–78. https://doi.org/10.1016/j.envpol.2018.11.061

Casini AF, Ferrali M, Pompella A, Maellaro E, Comporti M (1986). Lipid peroxidation and cellular damage in extrahepatic tissue of bromobenzene intoxicated mice. American Journal of Pathology, 123(3): 520–531.

Dallas LJ, Turner A, Bean TP, Lyons BP, Jha AN (2018). An integrated approach to assess the impacts of zinc pyrithione at different levels of biological organization in marine mussels. Chemosphere, 196: 531–539. https://doi.org/10.1016/j.chemosphere.2017.12.144

Erdoğan K (2023). Determination of acute toxicity of sodium pyrithione and its exposure effects on antioxidant enzymes activity, immune status, and histopathological changes in common carp. Chemistry and Ecology, 39(4): 376–392. https://doi.org/10.1080/02757540.2023.2198509

EU ECHA (European Chemicals Agency) (2026). Registration dossier: sodium pyrithione. Available at: https://echa.europa.eu/et/registration-dossier/-/registered-dossier/20845/7/7/1 (accessed 03 January 2026).

FDA (Food and Drug Administration) (2026). Environmental decisions. Available at: http://www.fda.gov/Food/IngredientsPackagingLabeling/EnvironmentalDecisions/default.htm (accessed 03 June 2026).

Firth DC, Salie K, O’Neill B, Hoffman LC (2019). Monitoring of trace metal accumulation in two South African farmed mussel species, Mytilus galloprovincialis and Choromytilus meridionalis. Marine Pollution Bulletin, 141: 529–534. https://doi.org/10.1016/j.marpolbul.2019.03.007

Flohe L, Günzler WA (1984). Assays of glutathione peroxidase. Methods in Enzymology, 105: 114–120. https://doi.org/10.1016/S0076-6879(84)05015-1

Jeong H, Ra K, Won JH (2021). A nationwide survey of trace metals and Zn isotopic signatures in mussels (Mytilus edulis) and oysters (Crassostrea gigas) from the coast of South Korea. Marine Pollution Bulletin, 173: 113061. https://doi.org/10.1016/j.marpolbul.2021.113061

Katalay S, Guner A, Dagdeviren M, Yigitturk G, Yavasoglu A, Gunal AC, et al. (2022). Oxidative stress-induced apoptotic changes after acute exposure to antifouling agent zinc pyrithione (ZnPT) in Mytilus galloprovincialis Lamark (Mediterranean mussels) tissues. Chemistry and Ecology, 38(4): 356–373. https://doi.org/10.1080/02757540.2022.2047951

Kattstrom D, Borenius A, Ruden C, Agerstrand M (2022). Stricter regulation applies to antimicrobial substances when used as biocides compared to cosmetics under current EU legislation. Emerging Contaminants, 8: 229–242. https://doi.org/10.1016/j.emcon.2022.04.003

Khan MI, Zahoor M, Khan A, Gulfam N, Khisroon M (2019). Bioaccumulation of heavy metals and their genotoxic effect on freshwater mussel. Bulletin of Environmental Contamination and Toxicology, 102(1): 52–58. https://doi.org/10.1007/s00128-018-2492-4

Kosnik MB, Hauschild MZ, Fantke P (2022). Toward assessing absolute environmental sustainability of chemical pollution. Environmental Science and Technology, 56: 4776–4787. https://doi.org/10.1021/acs.est.1c06098

Kurtel HI, Granger DN, Tso PA, Grisham MB (1992). Vulnerability of intestinal interstitial fluid to oxidant stress. American Journal of Physiology-Gastrointestinal and Liver Physiology, 263(4): G573–G578. https://doi.org/10.1152/ajpgi.1992.263.4.G573

Lesser MP (2006). Oxidative stress in marine environments: biochemistry and physiological ecology. Annual Review of Physiology, 68: 253–278. https://doi.org/10.1146/annurev.physiol.68.040104.110001

Li D, Pan B, Chen L, Wang Y, Wang T, Wang J, et al. (2021). Bioaccumulation and human health risk assessment of trace metals in the freshwater mussel Cristaria plicata in Dongting Lake, China. Journal of Environmental Sciences, 104: 335–350. https://doi.org/10.1016/j.jes.2020.12.012

OECD (Organization for Economic Co-operation and Development) (1993). OECD Guidelines for Testing of Chemicals. OECD, Paris.

Paglia DE, Valentine WN (1967). Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. Journal of Laboratory and Clinical Medicine, 70(1): 158–169.

Parihar MS, Javeri T, Hemnani T, Dubey AK, Prakash P (1997). Responses of superoxide dismutase, glutathione peroxidase and glutathione antioxidant defenses in gills of the freshwater catfish (Heteropneustes fossilis) to short-term elevated temperature. Journal of Thermal Biology, 22: 151–156. https://doi.org/10.1016/S0306-4565(97)00006-5

Piwowar A (2010). Advanced oxidation protein products. Part I. Mechanism of the formation, characteristics and property. Polski Merkuriusz Lekarski, 28(164): 166–169.

Santovito G, Trentin E, Gobbi I, Bisaccia P, Tallandini L, Irato P (2021). Non-enzymatic antioxidant responses of Mytilus galloprovincialis: insights into the physiological role against metal-induced oxidative stress. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 240: 108909. https://doi.org/10.1016/j.cbpc.2020.108909

SCCS (Scientific Committee on Consumer Safety) (2014). Opinion on Zinc Pyrithione, SCCS/1512/13, revision of 18 June 2014. European Commission, Brussels.

Sun Y, Oberley LW, Li Y (1988). A simple method for clinical assay of superoxide dismutase. Clinical Chemistry, 34(3): 497–500. https://doi.org/10.1093/clinchem/34.3.497

Swedish Chemicals Agency (2019). Proposal for Harmonised Classification and Labelling for a Biocidal Active Substance. CLH Report. Sodium pyrithione; Pyridine-2-thiol 1-oxide, sodium salt; pyrithione sodium. Regulation (EC) No 1272/2008 (CLP Regulation), Annex VI, Part 2, Version No. 2, March 2019. Available at: https://echa.europa.eu/documents/10162/e41c9e54-f4a8-d914-e69d-5f12c869b9b0 (accessed 03 June 2026).

Thakur D, Ganguly R (2022). Biocides. In: Hashmi MZ, Wang S, Ahmed Z (Eds). Environmental Micropollutants. Elsevier, pp 81–90. https://doi.org/10.1016/B978-0-323-90555-8.00007-6

Třešňáková N, Günal AÇ, Başaran Kankılıç G, Paçal E, Tavşanoğlu ÜN, Uyar R, et al. (2020). Sub-lethal toxicities of zinc pyrithione, copper pyrithione alone and in combination to the indicator mussel species Unio crassus Philipsson, 1788 (Bivalvia, Unionidae). Chemistry and Ecology, 36(4): 292–308. https://doi.org/10.1080/02757540.2020.1735377

Turkish Official Gazette (Resmi Gazete) (1991). Su Kirliliği ve Kontrolü Yönetmeliği Numune Alma ve Analiz Metodları Tebliği. Zehirlilik Seyreltme Faktörü (ZSF) Tayini. Tarih: 7.1.1991, Sayı: 20106.

Turley AE, Isaacs KK, Wetmore BA, Karmaus AL, Embry MR, Krishan M (2019). Incorporating new approach methodologies in toxicity testing and exposure assessment for tiered risk assessment using the RISK21 approach: case studies on food contact chemicals. Food and Chemical Toxicology, 134: 110819. https://doi.org/10.1016/j.fct.2019.110819

U.S. EPA (United States Environmental Protection Agency) (1996). Reregistration Eligibility Decision (RED), Sodium Omadine. EPA 738-R-96-031. U.S. Office of Prevention, Pesticides and Toxic Substances, Washington, DC.

Van Hassel JH, Farris JL (2007). A review of the use of unionid mussels as biological indicators of ecosystem health. In: Farris JL, Van Hassel JH (Eds). Freshwater Bivalve Ecotoxicology. SETAC Press, Pensacola, FL, USA, pp 19–49.

Witko-Sarsat V, Friedlander M, Capeillere-Blandin C, Nguyen-Khoa T, Nguyen AT, Zingraff J, et al. (1996). Advanced oxidation protein products as a novel marker of oxidative stress in uremia. Kidney International, 49(5): 1304–1313. https://doi.org/10.1038/ki.1996.186

Yıldırım F, Yılmaz K, Uyar Z, Erkoç F (2017). Investigation of acute toxicity of sodium omadine on Dreissena polymorpha (Zebra Mussel). The Turkish Journal of Occupational/Environmental Medicine and Safety, 2(1): 123–123.

Yildirim Z, Ucgun NI, Yildirim F (2011). The role of oxidative stress and antioxidants in the pathogenesis of age-related macular degeneration. Clinics, 66(5): 743–746. https://doi.org/10.1590/S1807-59322011000500006

Yılmaz Sezer İ, Koçak G, Tural R, Günal AÇ, Sepici Dinçel A (2024). Environmental pollutant sodium omadine: toxic effects in zebra fish (Danio rerio). Toxicology Mechanisms and Methods, 34(3): 256–261. https://doi.org/10.1080/15376516.2023.2279717

Zhang L, Li Q, Bao Y, Tan Y, Lametsch R, Hong H, et al. (2024). Recent advances on characterization of protein oxidation in aquatic products: a comprehensive review. Critical Reviews in Food Science and Nutrition, 64(6): 1572–1591. https://doi.org/10.1080/10408398.2022.2117788