Effect of waterborne copper oxide nanoparticles and copper ions on guppy (Poecilia reticulata): Bioaccumulation and histopathology

Document Type : Original Article

Authors

1 Student Research Committee AND Environmental Health Research Center, Kurdistan University of Medical Sciences, Sanandaj, Iran

2 Environmental Health Research Center, Kurdistan University of Medical Sciences, Sanandaj, Iran

3 Department of Biostatistics, School of Public Health, Iran University of Medical Sciences, Tehran, Iran

4 Department of Medical Entomology, School of Medicine, Hamadan University of Medical Sciences, Hamadan, Iran

5 Department of Fisheries, School of Natural Resources, University of Kurdistan, Sanandaj, Iran

Abstract

The aim of the present study was to investigate the effect of copper oxide nanoparticles (CuO-NPs) and copper ions (Cu++) on guppy (Poecilia reticulata), in order to assess Cu uptake in the gill, and histopathology of gill and intestinal organs in semi-static regimes for 10 days. Guppy fish were assigned into three groups; one control group, and two experimental groups receiving 20 µg/l of either Cu++ or CuO-NPs in a semi-static aqueous culture for 10 days. Gill and intestinal tissue samples were obtained under a standard protocol for further histopathological examinations. The notable alterations observed in gill tissues in the experimental groups were aneurism, fusion, gill epithelial hyperplasia, increased mucous secretion, and necrosis. Noticeable anomalies in intestinal tissue were increase in the number of goblet cells, swelling of goblet cells, degeneration, vacuolation, necrosis, and erosion. Moreover, copper accumulation in gill tissue in the Cu++ treated group was higher than that in the CuO-NPs treated group. In contrast, the severity of histopathological damages in gill and intestinal tissues was greater in the CuO-NPs experimental group. 

Keywords


  1. Isani G, Falcioni ML, Barucca G, Sekar D, Andreani G, Carpene E, et al. Comparative toxicity of CuO nanoparticles and CuSO4 in rainbow trout. Ecotoxicol Environ Saf 2013; 97: 40-6.
  2. Lapointe D, Pierron F, Couture P. Individual and combined effects of heat stress and aqueous or dietary copper exposure in fathead minnows (Pimephales promelas). Aquat Toxicol 2011; 104(1-2): 80-5.
  3. Handy RD. Chronic effects of copper exposure versus endocrine toxicity: two sides of the same toxicological process? Comp Biochem Physiol A Mol Integr Physiol 2003; 135(1): 25-38.
  4. Mela M, Guiloski IC, Doria HB, Rabitto IS, da Silva CA, Maraschi AC, et al. Risks of waterborne copper exposure to a cultivated freshwater Neotropical catfish (Rhamdia quelen). Ecotoxicol Environ Saf 2013; 88: 108-16.
  5. Wang T, Long X, Liu Z, Cheng Y, Yan S. Effect of copper nanoparticles and copper sulphate on oxidation stress, cell apoptosis and immune responses in the intestines of juvenile Epinephelus coioides. Fish Shellfish Immunol 2015; 44(2): 674-82.
  6. Scott GR, Sloman KA. The effects of environmental pollutants on complex fish behaviour: integrating behavioural and physiological indicators of toxicity. Aquat Toxicol 2004; 68(4): 369-92.
  7. Wang T, Long X, Cheng Y, Liu Z, Yan S. A comparison effect of copper nanoparticles versus copper sulphate on juvenile epinephelus coioides: growth parameters, digestive enzymes, body composition, and histology as biomarkers. Int J Genomics 2015; 2015: 783021.
  8. Li Y, Liang J, Tao Z, Chen J. CuO particles and plates: Synthesis and gas-sensor application. Materials Research Bulletin 2004; 43(8-9): 2380-5.
  9. Carnes CL, Klabunde KJ. The catalytic methanol synthesis over nanoparticle metal oxide catalysts. Journal of Molecular Catalysis A: Chemical 2003; 194(1-2): 227-36.
  10. Sau TK, Rogach AL, Jackel F, Klar TA, Feldmann J. Properties and applications of colloidal nonspherical noble metal nanoparticles. Adv Mater 2010; 22(16): 1805-25.
  11. Borkow G, Zatcoff RC, Gabbay J. Reducing the risk of skin pathologies in diabetics by using copper impregnated socks. Med Hypotheses 2009; 73(6): 883-6.
  12. Borkow G, Gabbay J, Dardik R, Eidelman AI, Lavie Y, Grunfeld Y, et al. Molecular mechanisms of enhanced wound healing by copper oxide-impregnated dressings. Wound Repair Regen 2010; 18(2): 266-75.
  13. Abdel-Khalek AA, Badran SR, Marie MS. Toxicity evaluation of copper oxide bulk and nanoparticles in Nile tilapia, Oreochromis niloticus, using hematological, bioaccumulation and histological biomarkers. Fish Physiol Biochem 2016.
  14. Shaw BJ, Al-Bairuty G, Handy RD. Effects of waterborne copper nanoparticles and copper sulphate on rainbow trout, (Oncorhynchus mykiss): physiology and accumulation. Aquat Toxicol 2012; 116-117: 90-101.
  15. Lakra WS, NagpureNS. Genotoxicological studies in fishes: A review. Indian J Anim Sci 2009; 79: 93-8.
  16. Tao S, Liu C, Dawson R, Long A, Xu F. Uptake of cadmium adsorbed on particulates by gills of goldfish (Carassius auratus). Ecotoxicol Environ Saf 2000; 47(3): 306-13.
  17. Griffitt RJ, Weil R, Hyndman KA, Denslow ND, Powers K, Taylor D, et al. Exposure to copper nanoparticles causes gill injury and acute lethality in zebrafish (Danio rerio). Environ Sci Technol 2007; 41(23): 8178-86.
  18. Al-bairuty GA. Histopathological effects of metal and metallic nanoparticles on the body systems of rainbow trout (Oncorhynchus mykiss) [PhD Thesis]. Plymouth, UK: School of Biomedical and Biological Sciences, University of Plymouth; 2013. p. 319.
  19. Hao L, Chen L, Hao J, Zhong N. Bioaccumulation and sub-acute toxicity of zinc oxide nanoparticles in juvenile carp (Cyprinus carpio): a comparative study with its bulk counterparts. Ecotoxicol Environ Saf 2013; 91: 52-60.
  20. Norouzi M, Mansouri B, Hamidian AH, Zarei I, Mansouri A. Metal concentrations in tissues of two fish species from Qeshm Island, Iran. Bull Environ Contam Toxicol 2012; 89(5): 1004-8.
  21. Majnoni F, Rezaei M, Mansouri B, Hamidian AH. Metal concentrations in tissues of common carp, Cyprinus carpio, and silver carp, Hypophthalmichthys molitrix from the Zarivar Wetland in Western Iran. Archives of Polish Fisheries 2013; 21(1): 11-8.
  22. Mansouri B, Maleki A, Johari SA, Reshahmanish N. Effects of cobalt oxide nanoparticles and cobalt ions on gill histopathology of zebrafish (Danio rerio). Aquaculture, Aquarium, Conservation & Legislation - International Journal of the Bioflux Society 2015; 8(3): 438-44.
  23. Tavana M, Kalbassi M R, Abedian Kenari A, Johari S A. Assessment of assimilation and elimination of silver and Tio2 nanoparticles in artemia franciscana in different salinities. Journal of Oceanography 2014; 5(19): 91-103.
  24. Zhao J, Wang Z, Liu X, Xie X, Zhang K, Xing B. Distribution of CuO nanoparticles in juvenile carp (Cyprinus carpio) and their potential toxicity. J Hazard Mater 2011; 197: 304-10.
  25. Griffitt RJ, Luo J, Gao J, Bonzongo JC, Barber DS. Effects of particle composition and species on toxicity of metallic nanomaterials in aquatic organisms. Environ Toxicol Chem 2008; 27(9): 1972-8.
  26. Mansouri B, Johari SA. Effects of short-term exposure to sublethal concentrations of silver nanoparticles on histopathology and electron microscope ultrastructure of zebrafish (danio rerio) gills. Iranian Journal of Toxicology 2016; 10(1): 15-20. [In Persian].
  27. Perera S, Pathiratne A. Haemato-immunological and histological responses in Nile tilapia, Oreochromisniloticus exposed to titanium dioxide nanoparticles. Sri Lanka J Aquat Sci 2012; 17: 1-18.
  28. Hassaninezhad L, Safahieh A, Salamat N, Savari A, Majd NE. Assessment of gill pathological responses in the tropical fish yellowfin seabream of Persian Gulf under mercury exposure. Toxicology Reports 2014; 1: 621-8.
  29. da Cruz AL, Prado TM, Maciel LA, Couto RD. Environmental effects on the gills and blood of Oreochromis niloticus exposed to rivers of Bahia, Brazil. Ecotoxicol Environ Saf 2015; 111: 23-31.
  30. Figueiredo-Fernandes A, Ferreira-Cardoso JV, Garcia-Santos S, Monteiro SM, Carrola J, Matos P, et al. Histopathological changes in liver and gill epithelium of Nile tilapia, Oreochromis niloticus, exposed to waterborne copper. Pesq Vet Bras 2007; 27(3): 103-9.
  31. iraungkoorskul W, Sahaphong S, Kangwanrangsan N. Toxicity of copper in butterfish (Poronotus triacanthus): tissues accumulation and ultrastructural changes. Environ Toxicol 2007; 22(1): 92-100.
  32. Griffitt RJ, Hyndman K, Denslow ND, Barber DS. Comparison of molecular and histological changes in zebrafish gills exposed to metallic nanoparticles. Toxicol Sci 2009; 107(2): 404-15.
  33. Subashkumar S, Selvanayagam M. First report on: Acute toxicity and gill histopathology of fresh water fish Cyprinus carpio exposed to Zinc oxide (ZnO) nanoparticles. Int J Sci Res 2014; 4(3): 1-4.
  34. Blanchard J, Grosell M. Copper toxicity across salinities from freshwater to seawater in the euryhaline fish Fundulus heteroclitus: is copper an ionoregulatory toxicant in high salinities? Aquat Toxicol 2006; 80(2): 131-9.
  35. Scown TM, Santos EM, Johnston BD, Gaiser B, Baalousha M, Mitov S, et al. Effects of aqueous exposure to silver nanoparticles of different sizes in rainbow trout. Toxicol Sci 2010; 115(2): 521-34.
  36. Srinonate A, Banlunara W, Maneewattanapinyo P, Thammacharoen C, Ekgasit S, Kaewamatawong T. Acute toxicity study of nanosilver particles in tilapia (oreochromis niloticus): pathological changes, particle bioaccumulation and metallothionien protein expression. Thai J Vet Med 2015; 45(1): 81-9.
  37. Federici G, Shaw BJ, Handy RD. Toxicity of titanium dioxide nanoparticles to rainbow trout (Oncorhynchus mykiss): gill injury, oxidative stress, and other physiological effects. Aquat Toxicol 2007; 84(4): 415-30.
  38. Chen J, Dong X, Xin Y, Zhao M. Effects of titanium dioxide nano-particles on growth and some histological parameters of zebrafish (Danio rerio) after a long-term exposure. Aquat Toxicol 2011; 101(3-4): 493-9.