Comparative Toxicity of Alpha and Gamma Iron Oxide Nanoparticles in Rainbow Trout: Histopathology, Hematology, Accumulation, and Oxidative Stress

Abstract

In this study, alpha and gamma iron oxide nanoparticles, characterizations, toxic effects after being exposed to rainbow trout (Oncorhynchus mykiss) at 0, 1, 10 and 25 mg/L concentrations for 10 days, and then 10-day recovery period without any nanoparticle exposure were examined for histopathological (kidney, liver and gill), hematological, iron accumulation and potential for oxidative stress (TBARS and GSH). Histopathological damages significant at the exposure of increasing concentrations of both nanoparticles (increase in melanomacrophage aggregations, epithelial tissue deformations, cytoplasmic vacuolizations, fatty changes, necrosis, pyknosis, hyperplasia, hypertrophy, lamellar fusions, capillary dilatations). Gamma nanoparticles were determined to accumulate more than the alpha nanoparticles. The most Fe accumulation was detected in the liver. The findings of oxidative stress parameters showed that both nanoparticles have the potential to generate oxidative stress. It was concluded that the exposure of alpha and gamma nanoparticles at specified concentrations and durations had a toxic effect on rainbow trout and the toxicity of these nanoparticles was similar.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Data Availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  1. Al-Bairuty, G. A., Shaw, B. J., Handy, R. D., & Henry, T. B. (2013). Histopathological effects of waterborne copper nanoparticles and copper sulphate on the organs of rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology, 126, 104–115. https://doi.org/10.1016/j.envint.2011.03.009.

    CAS  Article  Google Scholar 

  2. Ateş, M., Demir, V., Arslan, Z., Kaya, H., Yılmaz, S., & Camas, M. (2016). Chronic exposure of tilapia (Oreochromis niloticus) to iron oxide nanoparticles: Effects of particle morphology on accumulation, elimination, hematology and immune responses. Aquatic Toxicology, 177, 22–32. https://doi.org/10.1016/j.aquatox.2016.05.005.

    CAS  Article  Google Scholar 

  3. Blasco, J. & Corsi, I. (2019). Ecotoxicology of nanoparticles in aquatic systems. 1st ed. CRC Press 290 p.

  4. Can, M. M., Coşkun, M., & Fırat, T. A. (2012). Comparative study of nanosized iron oxide particles; magnetite (Fe3O4), maghemite (γ-Fe2O3) and hematite (α-Fe2O3), using ferromagnetic resonance. Journal of Alloys and Compounds, 542, 241–247. https://doi.org/10.1016/j.jallcom.2012.07.091.

    CAS  Article  Google Scholar 

  5. Dale, L. (2005). Synthesis, properties, and applications of iron nanoparticles. Small Nano Micro, 1, 482–501. https://doi.org/10.1002/smll.200500006.

    CAS  Article  Google Scholar 

  6. Demir, V., Ateş, M., Arslan, Z., Camas, M., Çelik, F., Bogatu, C., & Seyhaneyıldız, C. Ş. (2015). Influence of alpha and gamma-iron oxide nanoparticles on marine microalgae species. Bulletin of Environmental Contamination and Toxicology, 95, 752–757. https://doi.org/10.1007/s00128-015-1633-2.

    CAS  Article  Google Scholar 

  7. Federici, G., Shaw, B. J., & Handy, R. D. (2007). Toxicity of titanium dioxide nanoparticles to rainbow trout (Oncorhynchus mykiss): Gill injury, oxidative stress, and other physiological effects. Aquatic Toxicology, 84, 415–430. https://doi.org/10.1016/j.aquatox.2007.07.009.

    CAS  Article  Google Scholar 

  8. Garcia, A., Espinosa, R., Delgado, L., Casals, E., & Gonzalez, E. (2011). Acute toxicity of cerium oxide, titanium oxide and iron oxide nanoparticles using standardized tests. Desalination, 269, 136–141. https://doi.org/10.1016/j.desal.2010.10.052.

    CAS  Article  Google Scholar 

  9. Griffitt, R. J., Weil, R., Hyndman, K. A., Denslow, N. D., Powers, K., Taylor, D., & Barber, D. S. (2007). Exposure to copper nanoparticles causes gill injury and acute lethality in zebrafish (Danio rerio). Environmental Science & Technology, 41, 8178–8186. https://doi.org/10.1021/es071235e.

    CAS  Article  Google Scholar 

  10. Hao, L., Wang, Z., & Xing, B. (2009). Effect of sub-acute exposure to TiO2 nanoparticles on oxidative stress and histopathological changes in juvenile carp (Cyprinus carpio). Journal of Environmental Sciences, 21, 1459–1466. https://doi.org/10.1016/S1001-0742(08)62440-7.

    CAS  Article  Google Scholar 

  11. Hedayati, A., Hoseini, S. M., & Hoseinifar, S. H. (2016). Response of plasma copper, ceruloplasmin, iron and ions in carp, Cyprinus carpio to waterborne copper ion and nanoparticle exposure. Comparative Biochemistry and Physiology - Part C, 179, 87–93. https://doi.org/10.1016/j.cbpc.2015.09.007.

    CAS  Article  Google Scholar 

  12. Kadar, E., Lowe, D. M., Sole, M., Fisher, A. S., & Jha, A. N. (2010). Uptake and biological responses to nano-Fe versus soluble FeCl3 in excised mussel gills. Analytical and Bioanalytical Chemistry, 396, 657–666. https://doi.org/10.1007/s00216-009-3191-0.

    CAS  Article  Google Scholar 

  13. Kaya, H., Aydın, F., Gürkan, M., Yılmaz, S., Ateş, M., Demir, V., & Arslan, Z. (2015). A comparative toxicity study between small and large size zinc oxide nanoparticles in tilapia (Oreochromis niloticus): Organ pathologies, osmoregulatory responses and immunological parameters. Chemosphere, 144, 571–582. https://doi.org/10.1016/j.chemosphere.2015.09.024.

    CAS  Article  Google Scholar 

  14. Keerthika, V., Ramesh, R., & Rajan, M. R. (2017). Toxicity assessment of iron oxide nanoparticles in Labeo rohita. International Journal of Fisheries and Aqutic Studies, 7, 5(4), 1–6.

    Google Scholar 

  15. Kehrer, J. (1993). P. (1993). Free radical as mediator of tissue injury and disease. Critical Reviews in Toxicology, 23, 21–48. https://doi.org/10.3109/10408449309104073.

    CAS  Article  Google Scholar 

  16. Kumar, N., Prabhu, P. A. J., Pal, A. K., Remya, S., Aklakur, M. D., Rana, R. S., Gupta, S., Raman, R. P., & Jadhao, S. B. (2011). Anti-oxidative and immuno-hematological status of tilapia (Oreochromis mossambicus) during acute toxicity test of endosulfan. Pesticide Biochemistry and Physiology, 99, 45–52. https://doi.org/10.1016/j.pestbp.2010.10.003.

    CAS  Article  Google Scholar 

  17. Li, L., Jiang, W., Luo, K., Song, H., Lan, F., Wu, Y., & Gu, Z. (2013). Superparamagnetic iron oxide nanoparticles as MRI contrast agents for non-invasive stem cell labeling and tracking. Theranostics, 3(8), 595. https://doi.org/10.7150/thno.5366.

    CAS  Article  Google Scholar 

  18. Nations, S., Wages, M., Canas, J. E., Maul, J., & Theodorakis, C. (2011). Acute effects of Fe2O3, TiO2, ZnO and CuO nanomaterials on Xenopus laevis. Chemosphere, 83, 1053–1061. https://doi.org/10.1016/j.chemosphere.2011.01.061.

    CAS  Article  Google Scholar 

  19. Oberdörster, E. (2004). Manufactured nanomaterials (Fullerenes, C60) induce oxidative stress in the brain of juvenile largemouth bass. Environmental Health Perspectives, 112, 1058–1062. https://doi.org/10.1289/ehp.7021.

    CAS  Article  Google Scholar 

  20. Ottoni, C. A., Neto, M. L., Léo, P., Ortolan, B. D., Barbieri, E., & De Souza, A. O. (2020). Environmental impact of biogenic silver nanoparticles in soil and aquatic organisms. Chemosphere, 239, 124698. https://doi.org/10.1016/j.chemosphere.2019.124698.

    CAS  Article  Google Scholar 

  21. Özgür, M. E., Ulu, A., Balcıoğlu, S., Özcan, I., Köytepe, S., & Ateş, B. (2018). The toxicity assessment of iron oxide (Fe3O4) nanoparticles on physical and biochemical quality of rainbow trout spermatozoon. Toxics, 6(4), 62. https://doi.org/10.3390/toxics6040062.

    CAS  Article  Google Scholar 

  22. Randrianantoandro, N., Mercier, A. M., Hervieu, M., & Greneche, J. M. (2001). Direct phase transformation from hematite to maghemite during high energy ball milling. Materials Letters, 47, 150–158. https://doi.org/10.1016/S0167-577X(00)00227-5.

    CAS  Article  Google Scholar 

  23. Rauchova, H., Drahota, Z., & Koudelova, J. (1999). The role of membrane fluidity changes and thiobarbituric acid-reactive substances production in the inhibition of cerebral cortex Na+/K+-ATPase activity. Physiological Research, 48, 73–78.

    CAS  Google Scholar 

  24. Sepici Dinçel, A., Sarıkaya, R., Selvi, M., Şahin, D., Benli, Ç. K., & Atalay Vural, S. (2007). How sublethal fenitrothion is toxic in carp (Cyprinus carpio L.) fingerlings. Toxicology Mechanisms and Methods, 17, 489–495. https://doi.org/10.1080/1537651070138422.

    Article  Google Scholar 

  25. Smith, C. J., Shaw, B. J., & Handy, R. D. (2007). Toxicity of single walled carbon nanotubes to rainbow trout, (Oncorhynchus mykiss): Respiratory toxicity, organ pathologies, and other physiological effects. Aquatic Toxicology, 82, 94–109. https://doi.org/10.1016/j.aquatox.2007.02.003.

    CAS  Article  Google Scholar 

  26. Soenen, S. J., & De Cuyper, M. (2010). Assessing iron oxide nanoparticle toxicity in vitro: current status and future prospects. Nanomedicine, 5, 1261–1275. https://doi.org/10.2217/nnm.10.106.

    CAS  Article  Google Scholar 

  27. Soto, K. F., Carrasco, A., Powell, T. G., Garza, K. M., & Murr, L. E. (2005). Comparative ın vitro cytotoxicity assessment of some manufactured nanoparticulate materials characterized by transmission electron microscopy. Journal of Nanoparticle Research, 7, 145–169. https://doi.org/10.1007/s11051-005-3473-1.

    CAS  Article  Google Scholar 

  28. Srinivasan, V., Bhavan, P. S., Rajkumar, G., Satgurunathan, T., & Muralisankar, T. (2016). Effects of dietary iron oxide nanoparticles on the growth performance, biochemical constituents and physiological stress responses of the giant freshwater prawn Macrobrachium rosenbergii post-larvae. International Journal of Fisheries and Aquatic Studies, 4(2), 170–182.

    Google Scholar 

  29. Villacis, R. A., José Filho, S., Piña, B., Azevedo, R. B., Pic-Taylor, A., Mazzeu, J. F., & Grisolia, C. K. (2017). Integrated assessment of toxic effects of maghemite (γ-Fe2O3) nanoparticles in zebrafish. Aquatic Toxicology, 191, 219–225. https://doi.org/10.1016/j.aquatox.2017.08.004.

    CAS  Article  Google Scholar 

  30. Wang, B., Feng, W. Y., Zhu, M. T., Wang, Y., & Wang, M. (2009). Neurotoxicity of low-dose repeatedly intranasal instillation of nano and submicron sized ferric oxide particles in mice. Journal of Nanoparticle Research, 11, 41–53. https://doi.org/10.1007/s11051-008-9452-6.

    CAS  Article  Google Scholar 

  31. Zhang, J. F., Shen, H., Wang, X. R., Wu, J. C., & Xue, Y. Q. (2004). Effects of chronic exposure of 2,4-dichlorophenol on the antioxidant system in liver of freshwater fish Carassius auratus. Chemosphere, 55, 167–174. https://doi.org/10.1016/j.chemosphere.2003.10.048.

    CAS  Article  Google Scholar 

  32. Zhang, Y., Zhu, L., Zhou, Y., & Chen, J. (2015). Accumulation and elimination of iron oxide nanomaterials in zebrafish (Danio rerio) upon chronic aqueous exposure. Journal of Environmental Sciences, 30, 223–230. https://doi.org/10.1016/j.jes.2014.08.024.

    CAS  Article  Google Scholar 

  33. Zhu, M. T., Feng, W. Y., Wang, B., Wang, T. C., & Gu, Y. Q. (2008). Comparative study of pulmonary responses to nano and submicron sized ferric oxide in rats. Toxicology, 247, 102–111.

    CAS  Article  Google Scholar 

Download references

Funding

Çanakkale Onsekiz Mart University Scientific Research Projects Commission (Project No: FBA-2016-1005).

Author information

Affiliations

Authors

Contributions

Mert Gürkan: study conception, histopathological analysis, manuscript preparation, drawing of figures. Selin Ertürk Gürkan: study conception, data analysis, oxidative stress parameters, and accumulation analysis. Sevdan Yılmaz: hematological analysis. Mehmet Ateş: nanoparticle characterization analysis.

Corresponding author

Correspondence to Mert Gürkan.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethics Approval

An official application was made to the Çanakkale Onsekiz Mart University, Animal Experiments Local Ethics Committee for the “Ethics Committee Permit Certificate” before starting the study. Experiments were started after the permit was obtained. All experiments were carried out by experts in accordance with ethical rules.

Code Availability

No code availability.

Additional information

Publisher’s Note

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

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gürkan, M., Gürkan, S.E., Yılmaz, S. et al. Comparative Toxicity of Alpha and Gamma Iron Oxide Nanoparticles in Rainbow Trout: Histopathology, Hematology, Accumulation, and Oxidative Stress. Water Air Soil Pollut 232, 37 (2021). https://doi.org/10.1007/s11270-021-04988-6

Download citation

Keywords

  • Alpha iron oxide
  • Gamma iron oxide
  • Nanoparticle
  • Toxicity
  • Oncorhynchus mykiss