1. bookVolume 20 (2020): Issue 3 (July 2020)
Journal Details
First Published
25 Nov 2011
Publication timeframe
4 times per year
Open Access

Effect of Different Levels of Copper Nanoparticles and Copper Sulfate on Morphometric Indices, Antioxidant Status and Mineral Digestibility in the Small Intestine of Turkeys

Published Online: 01 Aug 2020
Volume & Issue: Volume 20 (2020) - Issue 3 (July 2020)
Page range: 975 - 990
Received: 27 Aug 2019
Accepted: 09 Jan 2020
Journal Details
First Published
25 Nov 2011
Publication timeframe
4 times per year

It was hypothesized that dietary copper (Cu) nanoparticles, as a substitute for the commonly used copper sulfate, could contribute to lowering the dietary inclusion levels of Cu without compromising growth performance or reducing Cu digestibility and utilization in turkeys. An experiment was carried out on 648 one-day-old Hybrid Converter turkeys divided into 6 groups with 6 replicates per group in a two-factorial design with 3 dietary inclusion levels of Cu (20, 10 and 2 mg kg−1) and 2 dietary sources of Cu, copper sulfate and Cu nanoparticles (Cu-SUL and Cu-NPs, respectively). The apparent digestibility coefficients of minerals were determined after 6 weeks, and tissue samples were collected after 14 weeks of experimental feeding. A decrease in the dietary inclusion levels of Cu from 20 to 10 and 2 mg kg−1 did not reduce the body weights of turkeys at 42 and 98 days of age. In comparison with the remaining treatments, the lowest dietary inclusion level of Cu significantly decreased MDA concentrations in small intestinal tissue (P=0.002) and in the bursa of Fabricius (P=0.001). The replacement of Cu-SUL with Cu-NPs differentially modulated the redox status of selected tissues, i.e., enhanced SOD activity in small intestinal tissue (P=0.001) and decreased total glutathione levels in the bursa of Fabricius (P=0.005). In general, neither the different levels nor sources of additional dietary Cu (main factors) exerted negative effects on the histological structure of the duodenum and jejunum in turkeys. The intestinal digestibility of Cu increased with decreasing dietary Cu levels, and as a consequence, the highest apparent digestibility coefficient of Cu (and zinc) was noted in turkeys fed diets with the addition of 2 mg kg−1 Cu-NPs. Therefore, the environmental burden of excreted Cu was substantially reduced along with decreasing dietary Cu levels but it did not depend on the Cu source.


Adegbenjo A.A., Idowu O.M.O., Oso A.O., Adeyemi O.A., Aobayo R.A., Akinloye O.A., Jegede A.V., Osho S.O., Williams G.A. (2014). Effects of dietary supplementation with copper sulphate and copper proteinate on plasma trace minerals, copper residues in meat tissues, organs, excreta and tibia bone of cockerels. Slovak J. Anim. Sci., 47: 164–171.Search in Google Scholar

Aebi H. (1984). Catalase in vitro. Methods Enzymol., 105: 121–126.Search in Google Scholar

Anwar M.I., Awais M.M., Akhtar M., Navid M.T., Muhammad F. (2019). Nutritional and immunological effects of nano-particles in commercial poultry. World’s Pout. Sci. J., 75:262–271.Search in Google Scholar

Ajuwon O.R., Idowu O.M.O., Afolabi S.A., Kehinde B.O., Oguntola O.O., Olatunbosun K.O. (2011). The effects of dietary copper supplementation on oxidative and antioxidant systems in broiler chickens. Arch. Zootec., 60: 275–282.Search in Google Scholar

Albanese A., Tang P.S., Chan W.C.W. (2012). The effect of nanoparticle size, shape, and surface chemistry on biological systems. Annu. Rev. Biomed. Eng., 14: 1–16.Search in Google Scholar

Arias V.J., Koutsos E.A. (2006). Effect of copper source and level on intestinal physiology and growth of broiler chickens. Poult. Sci., 85: 999–1007.Search in Google Scholar

Awad W.A., Ghareeb K., Abdel-Raheem S., Bohm J. (2009). Effects of dietary inclusion of probiotic and synbiotic on growth performance, organ weights, and intestinal histomorphology of broiler chickens. Poult. Sci., 88: 49–55.Search in Google Scholar

Bao Y.M., Choct M., Iji P., Bruerton A. (2007). Effect of organically complexed copper. iron. manganese. and zinc on broiler performance. mineral excretion. and accumulation in tissues. J. Appl. Poultry Res., 16: 448–455.Search in Google Scholar

Bunglavan S.J., Dass A.K.G., Shrivastava S. (2014). Use of nanoparticles as feed additives to improve digestion and absorption in livestock. Livestock Res. Int., 2: 36–47.Search in Google Scholar

Crater J.S., Carrier R.L. (2010). Barrier properties of gastrointestinal mucus to nanoparticles transport Macromol. Biosci., 10: 1473-1483.Search in Google Scholar

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. (2006). Acute toxicological effects of copper nanoparticles in vivo. Toxicol. Lett., 163: 109–120.Search in Google Scholar

Chiou P.W.S., Chen C.L., Chen K.L., Wu C.P. (1999). Effect of high dietary copper on the morphology of gastro-intestinal tract in broiler chickens. Asian Austral. J. Anim. Sci., 12: 548–553.Search in Google Scholar

Cholewińska E., Juśkiewicz J., Ognik K. (2018a). Comparison of the effct of dietary copper nanoparticles and one copper (II) salt on the metabolic and immune status in a rat model. J. Trace Elem. Med Biol., 48: 111–117.10.1016/j.jtemb.2018.03.01729773169Search in Google Scholar

Cholewińska E., Ognik K., Fotschki B., Zduńczyk Z., Juśkiewicz J. (2018b). Comparison of the effect of dietary copper nanoparticles and one copper (II) salt on the copper biodistribution and gastrointestinal and hepatic morphology and function in a rat model. PLoS ONE, 13(5): e0197083.10.1371/journal.pone.0197083595154629758074Search in Google Scholar

EFSA, Panel on Additives and Products or Substances used in Animal Feed (FEEDAP). (2016). Revision of the currently authorised maximum copper content in complete feed. EFSA J. 14: 4563.Search in Google Scholar

Gangadoo S., Stanley D., Hughus R., Moore R.J., Chapman J. (2016). Nanoparticles in feed: Progress and prospects in poultry research. Trends Food Sci. Tech., 58: 115–126.Search in Google Scholar

Gonzales-Eguia A., Fu C.M., Lu F.Y., Lien T.F. (2009). Effects of nanocopper on copper availability and nutrients digestibility, growth performance and serum traits of piglets. Livest. Sci., 126: 122–129.Search in Google Scholar

Hill E.K., Li J. (2017). Current and future prospects for nanotechnology in animal production. J Anim. Sci. Biotechnol., 8: 26. DOI: 10.1186/s40104-017-0157-5.10.1186/s40104-017-0157-5535105428316783Search in Google Scholar

Hillery A.M., Jani P.U., Florence A.T. (1994). Comparative, quantitative study of lymphoid and nonlymphoid uptake of 60 nm polystyrene particles. J. Drug. Target., 2: 151–156.Search in Google Scholar

Jachak A., Lai S.K., Hida K., Suk J.S., Markovic N., Biswal S., Breysse P.N., Hanes J. (2012). Transport of metal oxide nanoparticles and single-walled carbon nanotubes in human mucus. Nanotoxicology 6: 614–622.Search in Google Scholar

Jani P., Halbert G.W., Langridge J., Florence A.T. (1990). Nanoparticle uptake by the rat gastrointestinal mucosa: quantitation and particle size dependency. J. Pharm. Pharmacol., 42: 821–826.Search in Google Scholar

Jankowski J., Kozłowski K., Ognik K., Zduńczyk Z., Otowski K., Sawosz E., Juśkiewicz J. (2019). Redox and immunological status of turkeys fed diets with different levels and sources of copper. Ann. Anim. Sci., 19: 215–227.Search in Google Scholar

Jegede A.V., Oduguwa O.O., Oso A.O., Fafiolu A.O., Idowu O.M.O., Nollet L. (2012). Growth performance, blood characteristics and plasma lipids of growing pullet fed dietary concentrations of organic and inorganic copper sources. Livest. Sci., 145: 298–302.Search in Google Scholar

Johnson E.L., Nicholoson J.L., Doerr J.A. (1985). Effect of dietary copper on litter microbial population and broiler performance. Br. Poult. Sci., 26: 171–177.Search in Google Scholar

Jóźwik A., Marchewka J., Strzałkowska N. Horbńanczuk J.O., Szumacher-Strabel M., Cieślak A., Lipińska-Palka P., Józefiak D., Kamińska A., Atanasov A.G. (2018). The effect of different levels of Cu, Zn and Mn nanoparticles in hen turkey diet on the activity of aminopeptidases. Molecules 23, 1150; doi:10.3390/molecules23051150.10.3390/molecules23051150610058729751626Search in Google Scholar

Karimi A., Sadeghi G., Vaziry A. (2011). The effect of copper in excess of the requirement during the starter period on subsequent performance of broiler chicks. J. Appl. Poult. Res., 20: 203–209.Search in Google Scholar

King J.C., Shames D.M., Woodhouse L.R. (2000). Zinc homeostasis in humans. J. Nutr., 130: 1360S–1366S.Search in Google Scholar

Lim H. S., Paik I. K. (2006). Effects of dietary supplementation of copper chelates in the form of methionine, chitosan and yeast in laying hens, Asian-Aust. J. Anim. Sci., 19: 1174–1178.Search in Google Scholar

Linder M.C., Hazegh-Azam M. (1996). Copper biochemistry and molecular biology. Am. J. Clin. Nutr., 63: 797–811.Search in Google Scholar

Mabe I., Rapp C., Bain M.M., Nys Y. (2003). Supplementation of a corn-soybean meal diet with manganese, copper, and zinc from organic or inorganic sources improves eggshell quality in aged laying hens. Poultry Sci., 82: 1902–1913.Search in Google Scholar

Majewski M., Ognik K., Zduńczyk P., Juśkiewicz J. (2017). Effect of dietary copper nanoparticles versus one copper (II) salt: analysis of vasoreactivity in a rat model. Pharmacol. Rep., 69: 1282–1268.Search in Google Scholar

Makarski B., Gortat M., Lechowski J., Żukiewicz-Sobczak W., Sobczak P., Zawiślak K. (2014). Impact of copper (Cu) at the dose of 50 mg on haematological and biochemical blood parameters in turkeys, and level of Cu accumulation in the selected tissues as a source of information on product safety for consumers. Ann. Agric. Environ. Med., 21: 567–570.Search in Google Scholar

McGill S., Smyth H.D.C. (2010). Disruption of the mucus barrier by topically applied exogenous particles. Mol. Pharmaceutics 7: 2280-2288.Search in Google Scholar

O’Connor J.M. (2001). Trace elements and DNA damage. Biochem. Soc. Trans., 39: 354–357.Search in Google Scholar

Ognik K., Wertelecki T. (2012). Effect of different vitamin E sources and levels on selected oxidative status indices in blood and tissues as well as on rearing performance of slaughter turkey hens. J. Appl. Poultry Res., 2: 259–271.Search in Google Scholar

Ognik K, Stępniowska A, Cholewińska E, Kozłowski K (2016). The effect of administration of copper nanoparticles to chickens in drinking water on estimated intestinal absorption of iron, zinc, and calcium. Poult. Sci., 95: 2045-2051.Search in Google Scholar

Ognik K., Sembratowicz I., Cholewińska E., Jankowski J., Kozłowski K., Juśkiewicz J., Zduńczyk Z. (2018). The effect of administration of copper nanoparticles to chickens in their drinking water on the immune and antioxidant status of blood. Anim. Sci. J., 89: 579–588.Search in Google Scholar

Ognik K., Cholewińska E., Juśkiewicz J., Zduńczyk Z., Tutaj K., Szlązak R. (2019). The effect of copper nanoparticles and copper (II) salt on redox reactions and epigenetic changes in a rat model. J. Anim. Physiol. Anim. Nutr., 103: 675–686.Search in Google Scholar

Ognik K., Cholewińska E., Stępniowska A., Drażbo A., Kozłowski K., Jankowski J. (2019). The effect of administration of copper nanoparticles in drinking water on redox reactions in the liver and breast muscle of broiler chickens. Ann. Anim. Sci., 19: 663–677.Search in Google Scholar

Omaye S.T., Tumbull J.D., Sauberlich H.E. (1979). Selected methods for determination of ascorbic acid in animal cells, tissues and fluids. Meth. Enzymol., 62: 3–11.Search in Google Scholar

Otowski K., Ognik K., Kozłowski K. (2019). Growth rate, metabolic parameters and carcass quality in turkeys fed diets with different inclusion levels and sources of supplemental copper. J. Anim. Feed Sci., 28: 272–281.Search in Google Scholar

Pekel A., Alp M. (2011). Effects of different dietary copper sources on laying hen performance and egg yolk cholesterol. J. Appl. Poult. Res., 20: 506–513.Search in Google Scholar

Samanta B., Ghosh P.R., Biswas A., Das S.K. (2011). The effects of copper supplementation on the performance and hematological parameters of broiler chickens. Asian-Aust. J. Anim. Sci., 24: 1001–1006.Search in Google Scholar

Sawosz E., Łukasiewicz M., Łozicki A., Sosnowska M., Jaworski S., Niemiec J., Scott A., Jankowski J., Józefiak D., Chwalibog A. (2018). Effect of copper nanoparticles on the mineral content of tissues and droppings, and growth of chickens. Archiv. Animal Nutr. https://doi.org/10.1080/1745039X.2018.150514610.1080/1745039X.2018.150514630183391Search in Google Scholar

Schoendorfer N., Davies P.S.W. (2012). Micronutrients interrelationships: synergism and antagonism. In: Micronutrients. Betencourt A.I. Gaitan H.F. (eds), pp. 159–179.Search in Google Scholar

Scott A., Vadalasetty K.P., Chwalibog A., Sawosz E. Copper nanoparticles as an alternative feed additive in poultry diet: a review. Nanotechnol Rev 2018; 7(1): 69–93,10.1515/ntrev-2017-0159Search in Google Scholar

Smulikowska S., Rutkowski A. (2005). Recommended Allowances and Nutritive Value of Feedstuffs - Poultry Feeding Standards (in Polish). 5th ed. Smulikowska, S., Rutkowski, A., Eds. The Kielanowski Institute of Animal Physiology and Nutrition, Jablonna, PAS Polish.Search in Google Scholar

Sukalski K.A., LaBerge T.P., Johnson W.T. (1997). In vivo oxidative modification of erythrocyte membrane proteins in copper deficiency. Free Radic. Biol. Med., 22: 835–842.Search in Google Scholar

Yang F., Zhao L., Peng X., Deng J.L., Cui H.M. (2009). Effect of dietary high copper on the bursa of Fabricius in ducklings. Chin. J. Vet. Sci., 29: 354–359.Search in Google Scholar

Recommended articles from Trend MD

Plan your remote conference with Sciendo