Effect of different levels of copper nanoparticles and copper sulfate on morphometric indices, antioxidant status and mineral digestibility in the small intestine of turkeys

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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.

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  • 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.

  • Aebi H. (1984). Catalase in vitro. Methods Enzymol. 105: 121–126.

  • 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.

  • 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.

  • 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.

  • 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.

  • 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.

  • 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.

  • 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.

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

  • 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.

  • 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.

  • 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.

  • 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.

  • 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.

  • 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.

  • 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.

  • 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.

  • 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.

  • 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.

  • 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.

  • 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.

  • 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.

  • 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.

  • 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.

  • 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.

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

  • 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.

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

  • 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.

  • 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.

  • 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.

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

  • O’Connor J.M. (2001). Trace elements and DNA damage. Biochem. Soc. Trans. 39: 354–357.

  • 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.

  • 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.

  • 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.

  • 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.

  • 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.

  • 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.

  • 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.

  • 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.

  • 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.

  • 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.2018.1505146

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

  • 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

  • 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.

  • 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.

  • 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.

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