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Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Dietary supplementation with copper oxide nanoparticles ameliorates chronic heat stress in broiler chickens

Seham El-Kassas https://orcid.org/0000-0001-8083-6876 A H , Karima El-Naggar B , Safaa E. Abdo C , Walied Abdo D , Abeer A. K. Kirrella E , Ibrahim El-Mehaseeb F and Mohammed Abu El-Magd G
+ Author Affiliations
- Author Affiliations

A Animal, Poultry and Fish Breeding and Production, Department of Animal Wealth Development, Faculty of Veterinary Medicine, Kafrelsheikh University, Post Box 33516, Egypt.

B Department of Nutrition and Veterinary Clinical Nutrition, Faculty of Veterinary Medicine, Alexandria University, Post Box 22758, Egypt.

C Genetics and Genetic Engineering, Department of Animal Wealth Development, Faculty of Veterinary Medicine, Kafrelsheikh University, Post Box 33516, Egypt.

D Department of Pathology, Faculty of Veterinary Medicine, Kafrelsheikh University, Post Box 33516, Egypt.

E Poultry Physiology, Poultry production Department, Faculty of Agriculture, Kafrelsheikh University.

F Nano-chemistry Laboratory, Chemistry Department, Faculty of Science, Kafrelsheikh University, Post Box 33516, Egypt.

G Department of Anatomy, Faculty of Veterinary Medicine, Kafrelsheikh University, Post Box 33516, Egypt.

H Corresponding author. Email: seham.elkassas@vet.kfs.edu.eg; seham.elkassas7@gmail.com

Animal Production Science 60(2) 254-268 https://doi.org/10.1071/AN18270
Submitted: 26 April 2018  Accepted: 16 March 2019   Published: 6 December 2019

Abstract

Aims: Heat stress (HS) is one of the most serious problems of poultry production. Copper (Cu) is an essential trace element that plays a crucial role in the organism defence against oxidative stress. Because of the low mineral availability of the commercial Cu salts, in a novel approach, copper oxide nanoparticles (CuO-NPs) were used to alleviate chronic heat stress-induced degenerative changes in two commercial broiler strains (Ross 308 and Cobb 500).

Methods: Birds of each broiler strain were divided into six groups, with three replicates each. The first group (N1) received 100% of the recommended Cu requirements as CuO and was housed under normal temperature (24 ± 2°C), the second and third groups (N2 and N3 respectively) received 100% and 50% of the recommended Cu requirements as CuO-NPs and were housed under normal temperature. The fourth, fifth and sixth groups (H1, H2 and H3 respectively) received the same level of Cu supplementation as did the first, second and third groups respectively, and they were housed under normal temperature until the age of 21 days, and then exposed to HS (33 ± 2°C/5 h per day for two successive weeks).

Key results: Dietary supplementation with CuO-NPs during HS altered the HS-induced responses of the birds, as confirmed by decreased liver malondehyde (MDA) concentration and enhanced superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPx1) mRNA expression levels and enzyme activities (P < 0.001), with a distinct linear association between the gene expression level and enzyme activity. Copper oxide NPs also reduced HS-induced degenerative changes in the hepatic tissue. These nanoparticles modulated, although variably, liver HS protein 70 (HSP70), HS protein 90 (HSP90) and HS factor 3 (HSF3) mRNA transcript levels among Ross and Cobb chickens following HS (P < 0.001). Performance of both strains under HS was improved (as shown by a marked reduction in body temperature (P < 0.001) and a higher bodyweight (P < 0.01)) when CuO-NPs were supplemented in the diet, especially for the birds receiving 50% of the recommended Cu requirement, with different responses being noted in the two strains studied.

Conclusion: CuO-NPs could be used as a good alternative source of Cu in poultry nutrition during summer.

Implications: Dietary supplementation of CuO-NPs, especially at 50% of the birds’ recommended requirement, during heat stress could enhance bird performance, lower bird temperature and increase its resistance to negative consequences of elevated temperature.

Additional keywords: antioxidants, commercial broilers, growth performance.


References

Abdo SE, El-Kassas S, El-Nahas AF, Mahmoud S (2017) Modulatory effect of monochromatic blue light on heat stress response in commercial broilers. Oxidative Medicine and Cellular Longevity 2017, 1351945

Adegbenjo A, Idowu O, Oso A, Adeyemi O, Sobayo R, Akinloye O, Jegede A, Osho S, Williams G (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. Czech Journal of Animal Science 47, 164–171.

Aebi H (1984) Catalase in vitro. Methods in Enzymology 105, 121–126.
Catalase in vitro.Crossref | GoogleScholarGoogle Scholar | 6727660PubMed |

Akbarian A, Michiels J, Degroote J, Majdeddin M, Golian A, Smet S (2016) Association between heat stress and oxidative stress in poultry; mitochondrial dysfunction and dietary interventions with phytochemicals. Journal of Animal Science and Biotechnology 7, 37
Association between heat stress and oxidative stress in poultry; mitochondrial dysfunction and dietary interventions with phytochemicals.Crossref | GoogleScholarGoogle Scholar | 27354915PubMed |

Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg ET (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecology and Management 259, 660–684.
A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests.Crossref | GoogleScholarGoogle Scholar |

Altan Ö, Pabuçcuoğlu A, Altan A, Konyalioğlu S, Bayraktar H (2003) Effect of heat stress on oxidative stress, lipid peroxidation and some stress parameters in broilers. British Poultry Science 44, 545–550.
Effect of heat stress on oxidative stress, lipid peroxidation and some stress parameters in broilers.Crossref | GoogleScholarGoogle Scholar | 14584844PubMed |

Aviagen (2014) ‘Ross 308 nutrient specification guide.’ Available at http://en.aviagen.com/assets/Tech_Center/Ross_Broiler/Ross-308-Broiler-PO-2014-EN.pdf [Verified March 2017]

Azad MA, Kikusato M, Zulkifli I, Toyomizu M (2013) Electrolysed reduced water decreases reactive oxygen species-induced oxidative damage to skeletal muscle and improves performance in broiler chickens exposed to medium-term chronic heat stress. British Poultry Science 54, 503–509.
Electrolysed reduced water decreases reactive oxygen species-induced oxidative damage to skeletal muscle and improves performance in broiler chickens exposed to medium-term chronic heat stress.Crossref | GoogleScholarGoogle Scholar | 23815735PubMed |

Bancroft JD, Cook HC, Beckstead JH (1994) ‘Manual of histological techniques and their diagnostic application.’ (Churchill Livingstone: Edinburgh, UK)

Brinker CJ, Scherer GW (2013) ‘Sol-gel science: the physics and chemistry of sol-gel processing.’ (Academic Press: Boston, MA)

Close W (1998) The role of trace mineral proteinates in pig nutrition. In ‘Biotechnology in the feed industry’. (Eds TP Lyons, KA Jacques) pp. 469–483. (Nottingham University Press: Nottingham, UK)

Cobb-Vantress (2015) ‘Cobb 500 nutrient specification guide ‘ Available at http://www.cobb-vantress.com/docs/default-source/cobb-500-guides/Cobb500_Broiler_Performance_And_Nutrition_Supplement.pdf [Verified March 2017]

Cohen J (2002) ‘Strategic role for copper.’ Available at https://www.micro.net/siteassets/research/poultry/2.2-strategic-role-for-copper-article.pdf [Verified November 2017]

Das T, Mondal M, Biswas P, Bairagi B, Samanta C (2010) Influence of level of dietary inorganic and organic copper and energy level on the performance and nutrient utilization of broiler chickens. Asian–Australasian Journal of Animal Sciences 23, 82–89.
Influence of level of dietary inorganic and organic copper and energy level on the performance and nutrient utilization of broiler chickens.Crossref | GoogleScholarGoogle Scholar |

Deuschle U, Weser U (1985) Copper and inflammation. In ‘Oncogenes and human cancer blood groups in cancer copper and inflammation human insulin’. pp. 97–130. (Springer: Berlin, Heidelberg, Germany)

Feng J, Zhang M, Zheng S, Xie P, Ma A (2008) Effects of high temperature on multiple parameters of broilers in vitro and in vivo. Poultry Science 87, 2133–2139.
Effects of high temperature on multiple parameters of broilers in vitro and in vivo.Crossref | GoogleScholarGoogle Scholar | 18809877PubMed |

Gaetke LM, Chow CK (2003) Copper toxicity, oxidative stress, and antioxidant nutrients. Toxicology 189, 147–163.
Copper toxicity, oxidative stress, and antioxidant nutrients.Crossref | GoogleScholarGoogle Scholar | 12821289PubMed |

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. Livestock Science 126, 122–129.
Effects of nanocopper on copper availability and nutrients digestibility, growth performance and serum traits of piglets.Crossref | GoogleScholarGoogle Scholar |

Hagfeldt A, Graetzel M (1995) Light-induced redox reactions in nanocrystalline systems. Chemical Reviews 95, 49–68.
Light-induced redox reactions in nanocrystalline systems.Crossref | GoogleScholarGoogle Scholar |

Halliwell B, Whiteman M (2004) Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean? British Journal of Pharmacology 142, 231–255.
Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean?Crossref | GoogleScholarGoogle Scholar | 15155533PubMed |

Han X-Y, Du W-L, Huang Q-C, Xu Z-R, Wang Y-Z (2012) Changes in small intestinal morphology and digestive enzyme activity with oral administration of copper-loaded chitosan nanoparticles in rats. Biological Trace Element Research 145, 355–360.
Changes in small intestinal morphology and digestive enzyme activity with oral administration of copper-loaded chitosan nanoparticles in rats.Crossref | GoogleScholarGoogle Scholar | 21882065PubMed |

Hascik P, Kacaniova M, Mihok M, Pochop J, Benczova E, Hlinku TA (2010) Performance of various broiler chicken hybrids fed with commercially produced feed mixtures. International Journal of Poultry Science 9, 1076–1082.
Performance of various broiler chicken hybrids fed with commercially produced feed mixtures.Crossref | GoogleScholarGoogle Scholar |

Hefnawy AE, El-Khaiat HM (2015) The importance of copper and the effects of its deficiency and toxicity in animal health. International Journal of Livestock Research 5,

Jäättela M (1999) Heat shock proteins as cellular lifeguards. Annals of Medicine 31, 261–271.
Heat shock proteins as cellular lifeguards.Crossref | GoogleScholarGoogle Scholar | 10480757PubMed |

Johnson MA, Fischer JG, Kays SE (1992) Is copper an antioxidant nutrient? Critical Reviews in Food Science and Nutrition 32, 1–31.
Is copper an antioxidant nutrient?Crossref | GoogleScholarGoogle Scholar | 1290583PubMed |

Jóźwik A, Marchewka J, Strzałkowska N, Horbańczuk JO, Szumacher-Strabel M, Cieślak A, Lipińska-Palka P, Józefiak D, Kamińska A, Atanasov AG (2018) The effect of different levels of Cu, Zn and Mn nanoparticles in hen turkey diet on the activity of aminopeptidases. Molecules (Basel, Switzerland) 23, 1150
The effect of different levels of Cu, Zn and Mn nanoparticles in hen turkey diet on the activity of aminopeptidases.Crossref | GoogleScholarGoogle Scholar |

Konca Y, Kirkpinar F, Mert S, Yurtseven S (2009) Effects of dietary ascorbic acid supplementation on growth performance, carcass, bone quality and blood parameters in broilers during natural summer temperature. Asian Journal of Animal and Veterinary Advances 4, 139–147.
Effects of dietary ascorbic acid supplementation on growth performance, carcass, bone quality and blood parameters in broilers during natural summer temperature.Crossref | GoogleScholarGoogle Scholar |

Lara LJ, Rostagno MH (2013) Impact of heat stress on poultry production. Animals 3, 356–369.
Impact of heat stress on poultry production.Crossref | GoogleScholarGoogle Scholar | 26487407PubMed |

Li JL, Sunde RA (2016) Selenoprotein transcript level and enzyme activity as biomarkers for selenium status and selenium requirements of chickens (Gallus gallus). PLoS One 11, e0152392
Selenoprotein transcript level and enzyme activity as biomarkers for selenium status and selenium requirements of chickens (Gallus gallus).Crossref | GoogleScholarGoogle Scholar | 27992557PubMed |

Lin H, Zhang H, Du R, Gu X, Zhang Z, Buyse J, Decuypere E (2005) Thermoregulation responses of broiler chickens to humidity at different ambient temperatures. II. Four weeks of age. Poultry Science 84, 1173–1178.
Thermoregulation responses of broiler chickens to humidity at different ambient temperatures. II. Four weeks of age.Crossref | GoogleScholarGoogle Scholar | 16156199PubMed |

Linder MC (1991) Copper and metabolic regulation. In ‘Biochemistry of copper’. pp. 241–300. (Springer US: Boston, MA)

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods (San Diego, Calif.) 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.Crossref | GoogleScholarGoogle Scholar |

Lobago F, Melese G, Mideksa B, Tibbo M (2003) Comparative performance of two broiler hybrids (Cobb-500 and Ross) under small-scale production system in Debre Zeit, central Ethiopia. Bulletin of Animal Health and Production in Africa 51, 83–93.

Lorentzen M, Maage A, Julshamn K (1998) Supplementing copper to a fish meal based diet fed to Atlantic salmon parr affects liver copper and selenium concentrations. Aquaculture Nutrition 4, 67
Supplementing copper to a fish meal based diet fed to Atlantic salmon parr affects liver copper and selenium concentrations.Crossref | GoogleScholarGoogle Scholar |

Lukaski HC, Hall CB, Marchello MJ (1995) Body temperature and thyroid hormone metabolism of copper-deficient rats. The Journal of Nutritional Biochemistry 6, 445–451.
Body temperature and thyroid hormone metabolism of copper-deficient rats.Crossref | GoogleScholarGoogle Scholar |

Maheshwari S (2013) Environmental impacts of poultry production. Poultry, Fisheries & Wildlife Sciences 1, 101
Environmental impacts of poultry production.Crossref | GoogleScholarGoogle Scholar |

Marques C, Guo W, Pereira P, Taylor A, Patterson C, Evans PC, Shang F (2006) The triage of damaged proteins: degradation by the ubiquitin-proteasome pathway or repair by molecular chaperones. The FASEB Journal 20, 741–743.
The triage of damaged proteins: degradation by the ubiquitin-proteasome pathway or repair by molecular chaperones.Crossref | GoogleScholarGoogle Scholar | 16469848PubMed |

Mashaly M, Hendricks G, Kalama M, Gehad A, Abbas A, Patterson P (2004) Effect of heat stress on production parameters and immune responses of commercial laying hens. Poultry Science 83, 889–894.
Effect of heat stress on production parameters and immune responses of commercial laying hens.Crossref | GoogleScholarGoogle Scholar | 15206614PubMed |

McDowell LR (1992) ‘Minerals in animal and human nutrition.’ (Academic Press Inc.: San Diego, CA)

Miroshnikov SA, Yausheva EV, Sizova EA, Miroshnikova EP (2015) Comparative assessment of effect of copper nano-and microparticles in chicken. Oriental Journal of Chemistry 31, 2327–2336.
Comparative assessment of effect of copper nano-and microparticles in chicken.Crossref | GoogleScholarGoogle Scholar |

Mroczek‐Sosnowska N, Łukasiewicz M, Wnuk A, Sawosz E, Niemiec J, Skot A, Jaworski S, Chwalibog A (2016) In ovo administration of copper nanoparticles and copper sulfate positively influences chicken performance. Journal of the Science of Food and Agriculture 96, 3058–3062.
In ovo administration of copper nanoparticles and copper sulfate positively influences chicken performance.Crossref | GoogleScholarGoogle Scholar | 26417698PubMed |

Mujahid A, Pumford NR, Bottje W, Nakagawa K, Miyazawa T, Akiba Y, Toyomizu M (2007) Mitochondrial oxidative damage in chicken skeletal muscle induced by acute heat stress. Journal of Poultry Science 44, 439–445.
Mitochondrial oxidative damage in chicken skeletal muscle induced by acute heat stress.Crossref | GoogleScholarGoogle Scholar |

Nerren JR, Swaggerty CL, MacKinnon KM, Genovese KJ, He H, Pevzner I, Kogut MH (2009) Differential mRNA expression of the avian-specific toll-like receptor 15 between heterophils from Salmonella-susceptible and-resistant chickens. Immunogenetics 61, 71–77.
Differential mRNA expression of the avian-specific toll-like receptor 15 between heterophils from Salmonella-susceptible and-resistant chickens.Crossref | GoogleScholarGoogle Scholar | 19002681PubMed |

NRC (1994) ‘Nutrient requirements of poultry.’ (National Research Council, National Academy Press: Washington, DC)

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. Poultry Science 95, 2045–2051.
The effect of administration of copper nanoparticles to chickens in drinking water on estimated intestinal absorption of iron, zinc, and calcium.Crossref | GoogleScholarGoogle Scholar | 27307476PubMed |

Pearton S, Norton D, Ip K, Heo Y, Steiner T (2005) Recent progress in processing and properties of ZnO. Journal of Vacuum Science and Technology. B, Microelectronics and Nonmeter Structures 50, 293–340.

Pesti GM, Bakalli RI (1996) Studies on the feeding of cupric sulfate pentahydrate and cupric citrate to broiler chickens. Poultry Science 75, 1086–1091.
Studies on the feeding of cupric sulfate pentahydrate and cupric citrate to broiler chickens.Crossref | GoogleScholarGoogle Scholar | 8878264PubMed |

Ponukalina E, Afanas’ eva G, Chesnokova N, Kirichuk V (2000) Lipid peroxidation and the antioxidant blood system in dynamics of pestilential and choleraic intoxication. Patologicheskaia Fiziologiia i Eksperimental’Naia Terapiia 17–18.

Rimoldi S, Lasagna E, Sarti FM, Marelli SP, Cozzi MC, Bernardini G, Terova G (2015) Expression profile of six stress-related genes and productive performances of fast and slow growing broiler strains reared under heat stress conditions. Meta Gene 6, 17–25.
Expression profile of six stress-related genes and productive performances of fast and slow growing broiler strains reared under heat stress conditions.Crossref | GoogleScholarGoogle Scholar | 26380816PubMed |

Scott A, Vadalasetty K, Łukasiewicz M, Jaworski S, Wierzbicki M, Chwalibog A, Sawosz E (2017) Effect of different levels of copper nanoparticles and copper sulphate on performance, metabolism and blood biochemical profiles in broiler chicken Journal of Animal Physiology and Animal Nutrition 102, 1–10.

Shao X-p, Liu W-b, Xu W-n, Xia W, Jiang Y-y (2010) Effects of dietary copper sources and levels on performance, copper status, plasma antioxidant activities and relative copper bioavailability in Carassius auratus gibelio. Aquaculture 308, 60–65.
Effects of dietary copper sources and levels on performance, copper status, plasma antioxidant activities and relative copper bioavailability in Carassius auratus gibelio.Crossref | GoogleScholarGoogle Scholar |

Singh P (2016) Use of nano feed additives in livestock feeding. International Journal of Livestock Research 6, 1–14.
Use of nano feed additives in livestock feeding.Crossref | GoogleScholarGoogle Scholar |

Skřivan M, Ševčíková S, Tůmová E, Skřivanová V, Marounek M (2002) Effect of copper sulphate supplementation on performance of broiler chickens, cholesterol content and fatty acid profile of meat. Czech Journal of Animal Science 47, 275–280.

Song Z, Zhu L, Zhao T, Jiao H, Lin H (2009) Effect of copper on plasma ceruloplasmin and antioxidant ability in broiler chickens challenged by lipopolysaccharide. Asian–Australasian Journal of Animal Sciences 22, 1400–1406.
Effect of copper on plasma ceruloplasmin and antioxidant ability in broiler chickens challenged by lipopolysaccharide.Crossref | GoogleScholarGoogle Scholar |

Surai P (2015a) Antioxidant systems in poultry biology: heat shock proteins. Journal of Animal Research and Nutrition 1, 1188

Surai P (2015b) Antioxidant systems in poultry biology: superoxide dismutase. Journal of Animal Research and Nutrition

Tan G-Y, Yang L, Fu Y-Q, Feng J-H, Zhang M-H (2010) Effects of different acute high ambient temperatures on function of hepatic mitochondrial respiration, antioxidative enzymes, and oxidative injury in broiler chickens. Poultry Science 89, 115–122.
Effects of different acute high ambient temperatures on function of hepatic mitochondrial respiration, antioxidative enzymes, and oxidative injury in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 20008809PubMed |

Tawfeek SS, Hassanin K, Youssef IMI (2014) The effect of dietary supplementation of some antioxidants on performance, oxidative stress, and blood parameters in broilers under natural summer conditions. Journal of World’s Poultry Research 4, 10–19.

Tomaszewska E, Muszyński S, Ognik K, Dobrowolski P, Kwiecień M, Juśkiewicz J, Chocyk D, Świetlicki M, Blicharski T, Gładyszewska B (2017) Comparison of the effect of dietary copper nanoparticles with copper (II) salt on bone geometric and structural parameters as well as material characteristics in a rat model. Journal of Trace Elements in Medicine and Biology 42, 103–110.
Comparison of the effect of dietary copper nanoparticles with copper (II) salt on bone geometric and structural parameters as well as material characteristics in a rat model.Crossref | GoogleScholarGoogle Scholar | 28595781PubMed |

Vijayakumar M, Balakrishnan V (2014) Effect of calcium phosphate nanoparticles supplementation on growth performance of broiler chicken. Indian Journal of Science and Technology 7, 1149–1154.

Xie J, Tang L, Lu L, Zhang L, Xi L, Liu HC, Odle J, Luo X (2014) Differential expression of heat shock transcription factors and heat shock proteins after acute and chronic heat stress in laying chickens (Gallus gallus). PLoS One 9, e102204
Differential expression of heat shock transcription factors and heat shock proteins after acute and chronic heat stress in laying chickens (Gallus gallus).Crossref | GoogleScholarGoogle Scholar | 25549355PubMed |

Yu BP (1994) Cellular defenses against damage from reactive oxygen species. Physiological Reviews 74, 139–162.
Cellular defenses against damage from reactive oxygen species.Crossref | GoogleScholarGoogle Scholar | 8295932PubMed |