Skip to main content
SpringerLink
Log in

How Does Cyphenothrin Affect the Freshwater Mussel as In Vitro and In Vivo Models?

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

Cyphenothrin, one of the synthetic pyrethroids, developed as an alternative to organophosphorus and carbamate pesticides. It is used in veterinary medicine and household application against insects. Due to the contamination of the aquatic ecosystems, non-target aquatic organisms are affected. The current study aimed to evaluate the cyphenothrin effects on in vitro and in vivo models of freshwater mussels Unio delicatus Lea, 1863. While antioxidant enzyme (glutathione) was measured in both models, the total hemocyte counts were only detected in vivo models after exposure to cyphenothrin (1 and 10 μg/L) for 24-h and 48-h exposure times. A decrease in total hemocyte count occurred depending on the dose and duration (p < 0.001). In both in vitro and in vivo models of gill and digestive gland tissues, higher glutathione levels were obtained at a dose of 10 μg/L compared to the control groups in both exposure times (p < 0.001). The results of the study suggest that the antioxidant parameters could represent biomarkers to evaluate the effects of pollutants on in vitro and in vivo models of freshwater mussels.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data Availability

The research has no associate data.

References

  • AlkanUçkun, A. (2018). Investigation of toxic metal contamination in water and sediments of Gölbaşı Lake (Adıyaman). Adıyaman University Journal of Science, 8(2), 129–140.

    Google Scholar 

  • Almeida, E. A., Bainy, A. C. D., Dafre, A. L., Gomes, O. F., Medeiros, M. H., & Di Mascio, P. (2005). Oxidative stress in digestive gland and gill of the brown mussel (Perna perna) exposed to air and re-submersed. Journal of Experimental Marine Biology and Ecology, 318(1), 21–30. https://doi.org/10.1016/j.jembe.2004.12.007

    Article  CAS  Google Scholar 

  • Andreyeva, A. Y., Efremova, E. S., & Kukhareva, T. A. (2019). Morphological and functional characterization of hemocytes in cultivated mussel (Mytilus galloprovincialis) and effect of hypoxia on hemocyte parameters. Fish & Shellfish Immunology, 89, 361–367. https://doi.org/10.1016/j.fsi.2019.04.017

    Article  CAS  Google Scholar 

  • Arslan, P., Yurdakok-Dikmen, B., Ozeren, S. C., Kuzukıran, O., & Filazi, A. (2021). In vitro effects of erythromycin and florfenicol on primary cell lines of Unio crassus and Cyprinus carpio. Environmental Science and Pollution Research, 28, 48408–48416. https://doi.org/10.1007/s11356-021-14139-3

    Article  CAS  Google Scholar 

  • Arslan, P. (2022). Determinations of the effects of cyfluthrin on the hemocytes parameters of freshwater mussel (Unio delicatus). Ege Journal of Fisheries and Aquatic Sciences, 39(1), 39–45.

    Article  Google Scholar 

  • Balbi, T., Ciacci, C., Grasselli, E., Smerilli, A., Voci, A., & Canesi, L. (2017). Utilization of Mytilus digestive gland cells for the in vitro screening of potential metabolic disruptors in aquatic invertebrates. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 191, 26–35. https://doi.org/10.1016/j.cbpc.2016.08.009

    Article  CAS  Google Scholar 

  • Barrick, A., Manier, N., Lonchambon, P., Flahaut, E., Jrad, N., Mouneyrac, C., & Châtel, A. (2019). Investigating a transcriptomic approach on marine mussel hemocytes exposed to carbon nanofibers: An in vitro/in vivo comparison. Aquatic Toxicology, 207, 19–28. https://doi.org/10.1016/j.aquatox.2018.11.020

    Article  CAS  Google Scholar 

  • Birmelin, C., Pipe, R. K., Goldfarb, P. S., & Livingstone, D. R. (1999). Primary cell-culture of the digestive gland of the marine mussel Mytilus edulis: A time-course study of antioxidant-and biotransformation-enzyme activity and ultrastructural changes. Marine Biology, 135(1), 65–75.

    Article  Google Scholar 

  • Bradford, M. M. (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.

    Article  CAS  Google Scholar 

  • Canesi, L., Borghi, C., Fabbri, R., Ciacci, C., Lorusso, L. C., Gall, G., & Vergani, L. (2007). Effects of 17β-estradiol on mussel digestive gland. General and Comparative Endocrinology, 153(1–3), 40–46. https://doi.org/10.1016/j.ygcen.2007.02.005

    Article  CAS  Google Scholar 

  • Canesi, L., Viarengo, A., Leonzio, C., Filippelli, M., & Gallo, G. (1999). Heavy metals and glutathione metabolism in mussel tissues. Aquatic Toxicology, 46(1), 67–76. https://doi.org/10.1016/S0166-445X(98)00116-7

    Article  CAS  Google Scholar 

  • de la Ballina, N. R., Francesco, M., Asunción, C., & Antonio, V. (2022). Bivalve haemocyte subpopulations: A review. Frontiers in Immunology, 13.https://doi.org/10.3389/fimmu.2022.826255.

  • Doyotte, A., Cossu, C., Jacquin, M. C., Babut, M., & Vasseur, P. (1997). Antioxidant enzymes, glutathione and lipid peroxidation as relevant biomarkers of experimental or field exposure in the gills and the digestive gland of the freshwater bivalve Unio tumidus. Aquatic Toxicology, 39(2), 93–110. https://doi.org/10.1016/S0166-445X(97)00024-6

    Article  CAS  Google Scholar 

  • Ellman, G. L. (1959). Tissue sulfhydryl groups. Archives of Biochemistry and Biophysics, 82(1), 70–77.

    Article  CAS  Google Scholar 

  • Ensley, S. M. (2018). Pyrethrins and pyrethroids. In Veterinary Toxicology Basic and Clinical Principles (pp. 515–520). Academic Press. https://doi.org/10.1016/B978-0-12-811410-0.00039-8

  • Erkmen, B., Caliskan, M., & Yerli, S. V. (2000). Histopathological effects of cyphenothrin on the gills of Lebistes reticulatus. Veterinary and Human Toxicology, 42(1), 5–7.

    CAS  Google Scholar 

  • Faggio, C., Tsarpali, V., & Dailianis, S. (2018). Mussel digestive gland as a model tissue for assessing xenobiotics: An overview. Science of the Total Environment, 636, 220–229. https://doi.org/10.1016/j.scitotenv.2018.04.264

    Article  CAS  Google Scholar 

  • Feng, D., Ke, C., Li, S., Lu, C., & Guo, F. (2009). Pyrethroids as promising marine antifoulants: Laboratory and field studies. Marine Biotechnology, 11(2), 153–160. https://doi.org/10.1007/s10126-008-9130-9

    Article  CAS  Google Scholar 

  • Gómez-Mendikute, A., Elizondo, M., Venier, P., & Cajaraville, M. P. (2005). Characterization of mussel gill cells in vivo and in vitro. Cell and Tissue Research, 321(1), 131–140. https://doi.org/10.1007/s00441-005-1093-9

    Article  Google Scholar 

  • Guzmán-Soto, I., McTiernan, C., Gonzalez-Gomez, M., Ross, A., Gupta, K., Suuronen, E. J., Mah, T. F., Griffith, M., & Alarcon, E. I. (2021). Mimicking biofilm formation and development: Recent progress in in vitro and in vivo biofilm models. Iscience, 24(5), 102443. https://doi.org/10.1016/j.isci.2021.102443

    Article  CAS  Google Scholar 

  • Günal, A. Ç., Tunca, S. K., Arslan, P., Gül, G., & SepiciDinçel, A. (2021). How does sublethal permethrin effect non-target aquatic organisms? Environmental Science and Pollution Research, 28, 52405–52417. https://doi.org/10.1007/s11356-021-14475-4

    Article  CAS  Google Scholar 

  • Gürkan, S. E. (2022). Impact of nickel oxide nanoparticles (NiO) on oxidative stress biomarkers and hemocyte counts of Mytilus galloprovincialis. Biological Trace Element Research. https://doi.org/10.1007/s12011-022-03189-4

    Article  Google Scholar 

  • Huang, Y., Lin, Z., Zhang, W., Pang, S., Bhatt, P., Rene, E. R., Kumar, A. J., & Chen, S. (2020). New insights into the microbial degradation of D-cyphenothrin in contaminated water/soil environments. Microorganisms, 8, 473. https://doi.org/10.3390/microorganisms8040473

    Article  CAS  Google Scholar 

  • Katalay, S., Guner, A., Dagdeviren, M., Yigitturk, G., Yavasoglu, A., Gunal, A. C., Karabay Yavasoglu, N. U., & Oltulu, F., (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, 1-18.https://doi.org/10.1080/02757540.2022.2047951.

  • Li, F., Liu, Z., Yao, L., Jiang, Y., Qu, M., Yu, Y., Gong, X., Tan, Z., & Li, Z. (2022). Immunotoxicity of perfluorooctanoic acid to the marine bivalve species Ruditapes philippinarum. Environmental Toxicology and Chemistry, 41(2), 426–436. https://doi.org/10.1002/etc.5263

    Article  CAS  Google Scholar 

  • Lopes-Lima, M., Gürlek, M. E., Kebapçı, Ü., Şereflişan, H., Yanık, T., Mirzajan, A., Neubert, E., Prie, V., Teixeira, A., Gomes-dos-Santos, A., Barros-Garcia, D., Bolotov, I. N., Kondakov, A. V., Vikhrev, I. V., Tomilova, A. A., Özcan, T., Altun, A., Gonçalves, D. V., Bogan, A. E., & Froufe, E. (2021). Diversity, biogeography, evolutionary relationships, and conservation of Eastern Mediterranean freshwater mussels (Bivalvia: Unionidae). Molecular Phylogenetics and Evolytion, 163, 107261. https://doi.org/10.1016/j.ympev.2021.107261

    Article  Google Scholar 

  • Lutnicka, H., Bogacka, T., & Wolska, L. (1999). Degradation of pyrethroids in an aquatic ecosystem model. Water Research, 33, 3441–3446. https://doi.org/10.1016/S0043-1354(99)00054-8

    Article  CAS  Google Scholar 

  • Nimet, J., Neves, M. P., Viana, N. P., de Arruda Amorim, J. P., & Luciana, R. (2020). Histopathological alterations in gills of a fish (Astyanax bifasciatus) in neotropical streams: Negative effects of riparian forest reduction and presence of pesticides. Environment Monitoring and Assessment, 192, 58. https://doi.org/10.1007/s10661-019-8030-y

    Article  CAS  Google Scholar 

  • Panfoli, I., Burlando, B., & Viarengo, A. (2020). Effects of heavy metals on phospholipase C in gill and digestive gland of the marine mussel Mytilus galloprovincialis Lam. Comparative Biochemistry and Physiology Part b: Biochemistry & Molecular Biology, 127(3), 391–397. https://doi.org/10.1016/s0305-0491(00)00272-8

    Article  Google Scholar 

  • Parolini, M., Quinn, B., Binelli, A., & Provini, A. (2011). Cytotoxicity assessment of four pharmaceutical compounds on the zebra mussel (Dreissena polymorpha) haemocytes, gill and digestive gland primary cell cultures. Chemosphere, 84(1), 91–100.

    Article  CAS  Google Scholar 

  • Ray, M., Bhunia, A. S., Bhunia, N. S., & Ray, S. (2013). Density shift, morphological damage, lysosomal fragility and apoptosis of hemocytes of Indian molluscs exposed to pyrethroid pesticides. Fish & Shellfish Immunology, 35(2), 499–512. https://doi.org/10.1016/j.fsi.2013.05.008

    Article  CAS  Google Scholar 

  • Regoli, F. (1998). Trace metals and antioxidant enzymes in gills and digestive gland of the Mediterranean Mussel Mytilus galloprovincialis. Archives Environmental Contamination and Toxicology, 34, 48–63. https://doi.org/10.1007/s002449900285

    Article  CAS  Google Scholar 

  • Samadian, H., Khastar, H., Ehterami, A., & Salehi, M. (2021). Bioengineered 3D nanocomposite based on gold nanoparticles and gelatin nanofibers for bone regeneration: In vitro and in vivo study. Scientific Reports, 11(1), 1–11. https://doi.org/10.1038/s41598-021-93367-6

    Article  CAS  Google Scholar 

  • Staley, Z. R., Harwood, V. J., & Rohr, J. R. (2015). A synthesis of the effects of pesticides on microbial persistence in aquatic ecosystems. Critical Reviews of Toxicology, 45(10), 813–836. https://doi.org/10.3109/10408444.2015.1065471

    Article  CAS  Google Scholar 

  • Stara, A., Pagano, M., Capillo, G., Fabrello, J., Sandova, M., Vazzana, I., Zuskova, E., Velisek, J., Matozzo, V., & Faggio, C. (2020). Assessing the effects of neonicotinoid insecticide on the bivalve mollusc Mytilus galloprovincialis. Science of the Total Environment, 700, 134914. https://doi.org/10.1016/j.scitotenv.2019.134914

    Article  CAS  Google Scholar 

  • Timpano, A. J., Jones, J. W., Beaty, B., Hull, M., Soucek, D. J., & Zipper, C. E. (2022). Combined effects of copper, nickel, and zinc on growth of a freshwater mussel (Villosa iris) in an environmentally relevant context. Aquatic Toxicology, 242, 106038. https://doi.org/10.1016/j.aquatox.2021.106038

    Article  CAS  Google Scholar 

  • USEPA/OPP, EFED. (2000). Pesticide Ecotoxicity Database, as cited in the ECOTOX database. Available from, as of July 31, 2018: https://cfpub.epa.gov/ecotox/.

  • Verlecar, X. N., Jena, K. B., & Chainy, G. B. N. (2008). Seasonal variation of oxidative biomarkers in gills and digestive gland of green-lipped mussel Perna viridis from Arabian Sea. Estuarine, Coastal and Shelf Science, 76(4), 745–752.

    Article  Google Scholar 

  • Xiao, S., Yu, H., Xie, Y., Guo, Y., Fan, J., & Yao, W. (2021). The anti-inflammatory potential of Cinnamomum camphora (L.) J. Presl essential oil in vitro and in vivo. Journal of Ethnopharmacology, 267, 113516. https://doi.org/10.1016/j.jep.2020.113516.

  • Wang, T., Huang, X., Jiang, X., Hu, M., Huang, W., & Wang, Y. (2019). Differential in vivo hemocyte responses to nano titanium dioxide in mussels: Effects of particle size. Aquatic Toxicology, 212, 28–36. https://doi.org/10.1016/j.aquatox.2019.04.012

    Article  CAS  Google Scholar 

  • Wilhelm Filho, D., Tribess, T., Gaspari, C., Claudio, F. D., Torres, M. A., & Magalhaes, A. R. M. (2001). Seasonal changes in antioxidant defenses of the digestive gland of the brown mussel (Perna perna). Aquaculture, 203(1–2), 149–158. https://doi.org/10.1016/S0044-8486(01)00599-3

    Article  CAS  Google Scholar 

  • Wu, H., & Wang, W. X. (2010). NMR-based metabolomic studies on the toxicological effects of cadmium and copper on green mussels Perna viridis. Aquatic Toxicology, 100(4), 339–345. https://doi.org/10.1016/j.aquatox.2010.08.005

    Article  CAS  Google Scholar 

  • Wu, W., Geist, J., Beggel, S., Schmitz, C., Milz, S., & Sternecker, K. (2022). Immunohistochemical detection of various proteoglycans in the extracellular matrix of zebra mussels. Fishes, 7(2), 74. https://doi.org/10.3390/fishes7020074

    Article  Google Scholar 

  • Yameogo, L., Tapsoba, J. M., & Calamari, D. (1991). Laboratory toxicity of potential blackfly larvicides on some African fish species in the Onchocerciasis Control Programme area. Ecotoxicology and Environmental Safety, 21(3), 248–256. https://doi.org/10.1016/0147-6513(91)90063-u

    Article  CAS  Google Scholar 

  • Yavuzcan, H. Y., & Benli, A. Ç. K. (2004). Nitrite toxicity to crayfish, Astacus leptodactylus, the effects of sublethal nitrite exposure on hemolymph nitrite, total hemocyte counts, and hemolymph glucose. Ecotoxicology and Environmental Safety, 59(3), 370–375. https://doi.org/10.1016/j.ecoenv.2003.07.007

    Article  CAS  Google Scholar 

  • Yücel, G., & Özkul, İA. (2016). Pathomorphological evaluation of toxic effect of cypermethrin and cyphenothrin in common carp. Ankara University Journal of Veterinary Medicine Faculty, 63(4), 401–406.

    Google Scholar 

  • Yurdakök-Dikmen, B., Arslan, P., Kuzukıran, Ö., Filazi, A., & Erkoç, F., (2018). Unio sp. primary cell culture potential in ecotoxicology research. Toxin Reviews, 37(1), 75–81. https://doi.org/10.1080/15569543.2017.1331360

  • Zhan, H., Huang, Y., Lin, Z., Bhatt, P., & Chen, S. (2020). New insights into the microbial degradation and catalytic mechanism of synthetic pyrethroids. Environmental Research, 18, 109138. https://doi.org/10.1016/j.envres.2020.109138

    Article  CAS  Google Scholar 

  • Zhu, K., Deng, C., Du, P., Liu, T., Piao, J., Piao, Y., Yang, M., & Chen, L. (2022). G6PC indicated poor prognosis in cervical cancer and promoted cervical carcinogenesis in vitro and in vivo. Reproductive Biology and Endocrinology, 20, 50(2022). https://doi.org/10.1186/s12958-022-00921-6.

Download references

Acknowledgements

Special thanks to Prof. Dr. A. Çağlan Günal for providing cyphenothrin, and to Prof. Dr. Aylin Sepici-Dinçel for providing the Ellman’s reagent.

Author information

Authors and Affiliations

  1. Science Faculty, Biology Department, Çankırı Karatekin University, Çankırı, Turkey

    Pınar Arslan

Authors
  1. Pınar Arslan
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

The author designed the study, performed the experiments, evaluated the results, and wrote the manuscript.

Corresponding author

Correspondence to Pınar Arslan.

Ethics declarations

Conflict of Interest

The author declares no competing interests.

Additional information

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Arslan, P. How Does Cyphenothrin Affect the Freshwater Mussel as In Vitro and In Vivo Models?. Water Air Soil Pollut 233, 386 (2022). https://doi.org/10.1007/s11270-022-05860-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-022-05860-x

Keywords

Search

Navigation