Histopathological effects of waterborne copper nanoparticles and copper sulphate on the organs of rainbow trout (Oncorhynchus mykiss)

Aquatic Toxicology

Volumn 126, Issue , 2013, Pages 104-115

  Al Bairuty, Genan A ^a   Shaw, Benjamin J ^a   Handy, Richard D ^a   Henry, Theodore B ^a,b  

^a UNIVERSITY OF PLYMOUTH   (United Kingdom)

^b UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Brain injury; Copper nanoparticles; Copper toxicity; Fish; Gill pathology; Hypoxia; Renal pathology

Indexed keywords

COPPER; COPPER NANOPARTICLE; COPPER SULFATE;

BRAIN; COPPER; FISH; HISTOPATHOLOGY; HYPOXIA;

ANEURYSM; ANIMAL TISSUE; ARTICLE; BOWMAN CAPSULE; BRAIN BLOOD VESSEL; CELL VACUOLE; CEREBELLUM; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISEASE SEVERITY; ENVIRONMENTAL EXPOSURE; FISH DISEASE; GOBLET CELL; HEPATITIS; HISTOPATHOLOGY; HYPERPLASIA; INTESTINE MUCOSA; JUVENILE ANIMAL; KIDNEY TUBULE DISORDER; MESENCEPHALON; NANOTOXICOLOGY; NECROSIS; NONHUMAN; NUCLEAR SHAPE; PERIKARYON; PRIORITY JOURNAL; SKELETAL MUSCLE; TELENCEPHALON;

ANIMAL STRUCTURES; ANIMALS; COPPER; COPPER SULFATE; NANOPARTICLES; ONCORHYNCHUS MYKISS; WATER POLLUTANTS, CHEMICAL;

ONCORHYNCHUS MYKISS;

EID: 84869128504     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2012.10.005     Document Type: Article

References (43)

1. Baker J.T.P. Histological and electron microscopical observations on copper poisoning in the winter flounder (Pseudopleuronectes americanus). Journal of the Fisheries Research Board of Canada 1969, 26:2785-2793.
2. Berntssen M.H.G., Aatland A., Handy R.D. Chronic dietary mercury exposure causes oxidative stress, brain lesions, and altered behaviour in Atlantic salmon (Salmo salar) parr. Aquatic Toxicology 2003, 65:55-72.
3. Berntssen M.H.G., Hylland K., Wendelaar Bonga S.E., Maage A. Toxic levels of dietary copper in Atlantic salmon (Salmo salar L.) parr. Aquatic Toxicology 1999, 46:87-99.
4. Bilberg K., Malte H., Wang T., Baatrup E. Silver nanoparticles and silver nitrate cause respiratory stress in eurasian perch (Perca fluviatilis). Aquatic Toxicology 2010, 96:159-165.
5. Campbell H.A., Handy R.D., Sims D.W. Increased metabolic cost of swimming and consequent alterations to circadian activity in rainbow trout (Oncorhynchus mykiss) exposed to dietary copper. Canadian Journal of Fisheries and Aquatic Sciences 2002, 59:768-777.
6. Campbell H.A., Handy R.D., Sims D.W. Shifts in a fish's resource holding power during a contact paired interaction: the influence of a copper-contaminated diet in rainbow trout. Physiological and Biochemical Zoology 2005, 78:706-714.
7. Chen Z., Meng H., Xing G., Chen C., Zhao Y., Jia G., Wang T., Yuan H., Ye C., Zhao F., Chai Z., Zhu C., Fang X., Ma B., Wan L. Acute toxicological effects of copper nanoparticles in vivo. Toxicology Letters 2006, 163:109-120.
8. Choi J.E., Kim S., Ahn J.H., Youn P., Kang J.S., Park K., Yi J., Ryu D.-Y. Induction of oxidative stress and apoptosis by silver nanoparticles in the liver of adult zebrafish. Aquatic Toxicology 2010, 100:151-159.
9. Clearwater S.J., Handy R.D., Hogstrand C. Interaction of dietborne metals with digestive proccesses of fishes. Toxicity of Dietborne Metals to Aquatic Organisms 2005, 205-225. SETAC Press, Pensacola, USA. J.S. Meyer, W.J. Adams, K.V. Brix, S.N. Luoma, D.R. Mount, W.A. Stubblefield, C.M. Wood (Eds.).
10. Dang Z., Lock R.A.C., Flik G., Bonga S.E.W. Metallothionein response in gills of Oreochromis mossambicus exposed to copper in fresh water. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 1999, 277:R320-R331.
11. Federici G., Shaw B.J., Handy R.D. Toxicity of titanium dioxide nanoparticles to rainbow trout (Oncorhynchus mykiss): gill injury, oxidative stress, and other physiological effects. Aquatic Toxicology 2007, 84:415-430.
12. Figueiredo-Fernandes A., Ferreira-Cardoso J.V., Garcia-Santos S., Monteiro S.M., Carrola J., Matos P., Fontaínhas-Fernandes A. Histopathological changes in liver and gill epithelium of Nile tilapia, Oreochromis niloticus, exposed to waterborne copper. Pesquisa Veterinária Brasileira 2007, 27:103-109.
13. 2+ reveals different binding sites of amiloride and CDPC on the apical Na channel of frog skin. Biochimica et Biophysica Acta: Biomembranes 1998, 1370:169-174.
14. Griffitt R.J., Weil R., Hyndman K.A., Denslow N.D., Powers K., Taylor D., Barber D.S. Exposure to copper nanoparticles causes gill injury and acute lethality in zebrafish (Danio rerio). Environmental Science and Technology 2007, 41:8178-8186.
15. Grosell M., Blanchard J., Brix K.V., Gerdes R. Physiology is pivotal for interactions between salinity and acute copper toxicity to fish and invertebrates. Aquatic Toxicology 2007, 84:162-172.
16. 64Cu uptake and distribution among tissues of the european eel (Anguilla anguilla). Comparative Biochemistry and Physiology - Part C: Pharmacology, Toxicology & Endocrinology 1996, 114:229-235.
17. Haaparanta A., Valtonen E.T., Hoffmann R., Holmes J. Do macrophage centres in freshwater fishes reflect the differences in water quality?. Aquatic Toxicology 1996, 34:253-272.
18. Handy R.D., von der Kammer F., Lead J.R., Hassellöv M., Owen R., Crane M. The ecotoxicology and chemistry of manufactured nanoparticles. Ecotoxicology 2008, 17:287-314.
19. Handy R.D. Chronic effects of copper exposure versus endocrine toxicity: two sides of the same toxicological process?. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology 2003, 135:25-38.
20. Handy R.D., Al-Bairuty G., Al-Jubory A., Ramsden C.S., Boyle D., Shaw B.J., Henry T.B. Effects of manufactured nanomaterials on fishes: a target organ and body systems physiology approach. Journal of Fish Biology 2011, 79:821-853.
21. Handy R.D., Cornelis G., Fernandes T., Tsyusko O., Decho A., Sabo-Attwood T., Metcalfe C., Steevens J.A., Klaine S.J., Koelmans A.A., Horne N. Ecotoxicity test methods for engineered nanomaterials: Practical experiences and recommendations from the bench. Environmental Toxicology and Chemistry 2012, 31:15-31.
22. Handy R.D., Maunder R.J. The biological roles of mucus: importance for osmoregulation and osmoregulatory disorders of fish health. Osmoregulation and Ion Transport: Integrating Physiological, Molecular and Environmental Aspects. Essential Reviews in Experimental Biology 2009, vol. 1:203-235. Society for Experimental Biology Press, London.
23. Handy R.D., Sims D.W., Giles A., Campbell H.A., Musonda M.M. Metabolic trade-off between locomotion and detoxification for maintenance of blood chemistry and growth parameters by rainbow trout (Oncorhynchus mykiss) during chronic dietary exposure to copper. Aquatic Toxicology 1999, 47:23-41.
24. 2 nanoparticles on oxidative stress and histopathological changes in juvenile carp (Cyprinus carpio). Journal of Environmental Sciences 2009, 21:1459-1466.
25. Hoyle I., Shaw B.J., Handy R.D. Dietary copper exposure in the African walking catfish, Clarias gariepinus: transient osmoregulatory disturbances and oxidative stress. Aquatic Toxicology 2007, 83:62-72.
26. Kahru A., Savolainen K. Potential hazard of nanoparticles: from properties to biological and environmental effects. Toxicology 2010, 269:89-91.
27. Klaine S.J., Alvarez P.J.J., Batley G.E., Fernandes T.F., Handy R.D., Lyon D.Y., Mahendra S., McLaughlin M.J., Lead J.R. Nanomaterials in the environment behavior, fate, bioavailability, and effects. Environmental Toxicology and Chemistry 2008, 27:1825-1851.
28. Kosai P., Jiraungkoorskul W., Thammasunthorn T., Jiraungkoorskul K. Reduction of copper-induced histopathological alterations by calcium exposure in Nile tilapia (Oreochromis niloticus). Toxicology Mechanisms and Methods 2009, 19:461-467.
29. Lanno R.P., Hicks B., Hilton J.W. Histological observations on intrahepatocytic copper-containing granules in rainbow trout reared on diets containing elevated levels of copper. Aquatic Toxicology 1987, 10:251-263.
30. Li H., Zhou Q., Wu Y., Fu J., Wang T., Jiang G. Effect of waterborne nano-iron on medaka (Oryzias latipes): antioxidant enzymatic activity, lipid peroxidation and histopathology. Ecotoxicology and Environment Safety 2009, 72:684-692.
31. Menkes J.H. Menkes disease and wilson disease: two sides of the same copper coin. Part II: Wilson disease. European Journal of Paediatric Neurology 1999, 3:245-253.
32. Moger J., Johnston B.D., Tyler C.R. Imaging metal oxide nanoparticles in biological structures with CARS microscopy. Optics Express 2008, 16:3408-3419.
33. Moore M.N. Do nanoparticles present ecotoxicological risks for the health of the aquatic environment?. Environment International 2006, 32:967-976.
34. Mustafa S.A., Davies S.J., Jha A.N. Determination of hypoxia and dietary copper mediated sub-lethal toxicity in carp, Cyprinus carpio, at different levels of biological organisation. Chemosphere 2012, 87:413-422.
35. Scown T.M., van Aerle R., Johnston B.D., Cumberland S., Lead J.R., Owen R., Tyler C.R. High doses of intravenously administered titanium dioxide nanoparticles accumulate in the kidneys of rainbow trout but with no observable impairment of renal function. Toxicological Sciences 2009, 109:372-380.
36. Sharma H.S., Hussain S., Schlager J., Ali S.F., Sharma A. Influence of nanoparticles on blood-brain barrier permeability and brain edema formation in rats. Acta Neurochirurgica Supplement 2010, 106:359-364.
37. Shaw B.J., Al-Bairuty G.A., Handy R.D. Effects of waterborne copper nanoparticles and copper sulphate on rainbow trout, (Oncorhynchus mykiss): physiology and accumulation. Aquatic Toxicology 2012, 116-117:90-101.
38. Shaw B.J., Handy R.D. Physiological effects of nanoparticles on fish: a comparison of nanometals versus metal ions. Environment International 2011, 37:1083-1097.
39. Smith C.J., Shaw B.J., Handy R.D. Toxicity of single walled carbon nanotubes to rainbow trout, (Oncorhynchus mykiss): respiratory toxicity, organ pathologies, and other physiological effects. Aquatic Toxicology 2007, 82:94-109.
40. Sola F., Isaia J., Masoni A. Efeects of copper on gill structure and transport function in the rainbow trout, Oncorhynchus mykiss. Journal of Applied Toxicology 1995, 15:391-398.
41. Vogel F.S. The deposition of exogenous copper under experimental conditions with observations on its neurotoxic and nephrotoxic properties in relation to Wilson's disease. Journal of Experimental Medicine 1959, 110:801-810.
42. Weibel E.R., Kistler G.S., Scherle W.F. Practical steriological methods for morphometric cytology. Journal of Cell Biology 1966, 30:23-38.
43. Wilson R.W., Taylor E.W. The physiological responses of freshwater rainbow trout, Oncorhynchus mykiss, during acutely lethal copper exposure. Journal of Comparative Physiology Part B - Biochemical, Systems, and Environmental Physiology 1993, 163:38-47.