Feeding antioxidant vitamin and vegetable oils to broilers: vitamin E reduced negative effect of soybean oil on immune response and meat lipid oxidation
M. Mohiti-Asli A B and M. Ghanaatparast-Rashti AA Department of Animal Science, Faculty of Agriculture Science, University of Guilan, 41635-1314, Rasht, Iran.
B Corresponding author. Email: mmohiti@guilan.ac.ir
Animal Production Science 58(10) 1829-1836 https://doi.org/10.1071/AN16677
Submitted: 17 October 2016 Accepted: 13 April 2017 Published: 24 May 2017
Abstract
This study investigated the effect of feeding vitamin E, vitamin C, and two sources of vegetable oil on immune response and meat quality of broilers. A total of 320 one-day-old chicks were used in a completely randomised design with eight treatments arranged as a 2 × 2 × 2 factorial with two levels of vitamin E (0 and 200 mg/kg), two levels of vitamin C (0 and 1000 mg/kg), and two sources of vegetable oil (soybean and canola). Dietary supplementation of either vitamin E or C increased (P < 0.05) secondary humoral response, whereas oil sources had no significant effect. Broilers fed soybean oil had lower cellular response to the phytohemagglutinin skin test than those fed canola oil in diet, and supplementation of vitamin E increased cellular immune response. However, fat, cholesterol and pH of meat were not affected by source of oil or antioxidants, lipid oxidation was higher (P < 0.05) in thigh and breast meat of broilers fed soybean oil than canola oil. Dietary supplementation of vitamin E decreased (P < 0.05) lipid oxidation in thigh and breast of broilers fed diet containing soybean oil, without any effect on meat oxidation of those fed canola oil. Dietary supplementation of vitamin C increased lipid oxidation in thigh meat of broilers (P < 0.05). It can be concluded that inclusion of soybean oil to the diet, compared with canola oil, increased need for antioxidant. Vitamin E had beneficial effects on immune response and reduced meat lipid oxidation; nonetheless future studies should explore the antioxidant effect of vitamin C in stored meat.
Additional keywords: chicken meat, dietary oils, immunity, meat quality, vitamin C.
References
Al-Masad M (2012) Effect of vitamin C and zinc on broilers performance of immunocompetence under heat stress. Asian Journal of Animal Sciences 6, 76–84.| Effect of vitamin C and zinc on broilers performance of immunocompetence under heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVyms7zL&md5=beef0f80cd4048dfcf71d665b162a77eCAS |
Alaoui El Azher M, Havet N, Singer M, Dumarey C, Touqui L (2000) Inhibition by unsaturated fatty acids of type II secretory phospholipase A2 synthesis in guinea‐pig alveolar macrophages. European Journal of Biochemistry 267, 3633–3639.
| Inhibition by unsaturated fatty acids of type II secretory phospholipase A2 synthesis in guinea‐pig alveolar macrophages.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3czpsFSlsg%3D%3D&md5=d1ecc5a81bc9d948706767c5c3479513CAS |
AOAC (Association of Official Analytical Chemists) (2005) ‘Official methods of analysis.’ 18th edn. (Association of Official Analytical Chemists: Gaithersburg, MD)
Bayraktar H, Altan O, Acikgoz Z, Baysal SH, Seremet C (2011) Effects of oxidised oil and vitamin E on performance and some blood traits of heat-stressed male broilers. South African Journal of Animal Science 41, 288–296.
Bhor VM, Raghuram N, Sivakami S (2004) Oxidative damage and altered antioxidant enzyme activities in the small intestine of streptozotocin-induced diabetic rats. The International Journal of Biochemistry & Cell Biology 36, 89–97.
| Oxidative damage and altered antioxidant enzyme activities in the small intestine of streptozotocin-induced diabetic rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXosVyhsbc%3D&md5=81747ebf0c8640eed467f30f6019da36CAS |
Biswas S, Das AK, Banerjee R, Sharma N (2007) Effect of electrical stimulation on quality of tenderstretched chevon sides. Meat Science 75, 332–336.
| Effect of electrical stimulation on quality of tenderstretched chevon sides.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MbnsF2lsA%3D%3D&md5=9da94c8edece39e42db8c26cff95c517CAS |
Botsoglou NA, Fletouris DJ, Papageorgiou GE, Vassilopoulos VN, Mantis AJ, Trakatellis AG (1994) Rapid, sensitive, and specific thiobarbituric acid method for measuring lipid peroxidation in animal tissue, food, and feedstuff samples. Journal of Agricultural and Food Chemistry 42, 1931–1937.
| Rapid, sensitive, and specific thiobarbituric acid method for measuring lipid peroxidation in animal tissue, food, and feedstuff samples.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlsFKjtrc%3D&md5=a9cb30de4aef553e9b2211f3f78ebdbeCAS |
Bou R, Codony R, Tres A, Decker EA, Guardiola F (2009) Dietary strategies to improve nutritional value, oxidative stability, and sensory properties of poultry products. Critical Reviews in Food Science and Nutrition 49, 800–822.
| Dietary strategies to improve nutritional value, oxidative stability, and sensory properties of poultry products.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1WhtL7F&md5=c8a650dfec3200e15db58b3bb6b11c0fCAS |
Carpenter MP (1981) Antioxidant effects on the prostaglandin endoperoxide synthetase product profile. Federation Proceedings 40, 189–194.
Carr AC, Zhu BZ, Frei B (2000) Potential antiatherogenic mechanisms of ascorbate (vitamin C) and α-tocopherol (vitamin E). Circulation Research 87, 349–354.
| Potential antiatherogenic mechanisms of ascorbate (vitamin C) and α-tocopherol (vitamin E).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXms1ynu70%3D&md5=f1fffa886d2734be4d6593fecc0106b7CAS |
Carrillo-Pérez C, Cavia Camarero MDM, Alonso de la Torre S (2012) Role of oleic acid in immune system; mechanism of action; a review. Nutricion Hospitalaria 27, 978–990.
Corrier DE (1990) Comparison of phytohemagglutinin-induced cutaneous hypersensitivity reactions in the interdigital skin of broiler and layer chicks. Avian Diseases 34, 369–373.
| Comparison of phytohemagglutinin-induced cutaneous hypersensitivity reactions in the interdigital skin of broiler and layer chicks.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3czhsV2jsw%3D%3D&md5=91fe27e4903492d90826e9ceeca8d84cCAS |
Corwin LM, Shloss J (1980) Influence of vitamin E on the mitogenic response of murine lymphoid cells. The Journal of Nutrition 110, 916–923.
Corwin LM, Gordon RK, Shloss J (1981) Studies of the mode of action of vitamin E in stimulating T-cell mitogenesis. Scandinavian Journal of Immunology 14, 565–571.
Crespo N, Esteve-Garcia E (2001) Dietary fatty acid profile modifies abdominal fat deposition in broiler chickens. Poultry Science 80, 71–78.
| Dietary fatty acid profile modifies abdominal fat deposition in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXitVKgtro%3D&md5=b31f1adae39e9964ca7976d843e700dfCAS |
Cury-Boaventura MF, Gorjao R, De Lima TM, Newsholme P, Curi R (2006) Comparative toxicity of oleic and linoleic acid on human lymphocytes. Life Sciences 78, 1448–1456.
| Comparative toxicity of oleic and linoleic acid on human lymphocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsFOit7Y%3D&md5=5685bd1ae8c44e038cf6a7ae19642ea2CAS |
De Hoff JL, Davidson LM, Kritchevsky D (1978) An enzymatic assay for determining free and total cholesterol in tissue. Clinical Chemistry 24, 433–435.
Decker EA, Xu Z (1998) Minimizing rancidity in muscle foods. Food Technology 52, 54–59.
Decker EA, Livisay SA, Zhou S (2000) Mechanisms of endogenous skeletal muscle antioxidants: chemical and physical aspects. In ‘Antioxidants in muscle foods: nutritional strategies to improve quality’. (Eds EA Decker, C Faustman, CJ Lopez-Bote) pp. 25–60. (Wiley Interscience: New York)
Florou-Paneri P, Giannenas I, Christaki E, Govaris A, Botsoglou N (2006) Performance of chickens and oxidative stability of the produced meat as affected by feed supplementation with oregano, vitamin C, vitamin E and their combinations. Archiv für Geflügelkunde 70, 232–239.
Gallardo MA, Pérez DD, Leighton FM (2012) Modification of fatty acid composition in broiler chickens fed canola oil. Biological Research 45, 149–161.
| Modification of fatty acid composition in broiler chickens fed canola oil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjsFyqsro%3D&md5=08aee2eaf76f147acfdb45d0813a84e7CAS |
Grau A, Guardiola F, Grimpa S, Barroeta AC, Codony R (2001) Oxidative stability of dark chicken meat through frozen storage: Influence of dietary fat and α-tocopherol and ascorbic acid supplementation. Poultry Science 80, 1630–1642.
| Oxidative stability of dark chicken meat through frozen storage: Influence of dietary fat and α-tocopherol and ascorbic acid supplementation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXpt1eit70%3D&md5=48b2216f94045daf152def24c7ce8663CAS |
Gross WB (1992) Effects of ascorbic acid on stress and disease in chickens. Avian Diseases 36, 688–692.
| Effects of ascorbic acid on stress and disease in chickens.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s%2FjvVentg%3D%3D&md5=8f5eda6e74f77ced858bbeb1b1589dbeCAS |
Gu JY, Wakizono Y, Sunada Y, Hung P, Nonaka M, Sugano M, Yamada K (1999) Dietary effect of tocopherols and tocotrienols on the immune function of spleen and mesenteric lymph node lymphocytes in Brown Norway rats. Bioscience, Biotechnology, and Biochemistry 63, 1697–1702.
| Dietary effect of tocopherols and tocotrienols on the immune function of spleen and mesenteric lymph node lymphocytes in Brown Norway rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnt1Gjsbo%3D&md5=dd8a48ee8e7cc5236b27672cc3d85ccbCAS |
Jensen C, Lauridsen C, Bertelsen G (1998) Dietary vitamin E: Quality and storage stability of pork and poultry. Trends in Food Science & Technology 9, 62–72.
| Dietary vitamin E: Quality and storage stability of pork and poultry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjtVOqsbs%3D&md5=babbcd3033f40a57f3fed54dd3aad60aCAS |
John JL (1994) The avian spleen: a neglected organ. The Quarterly Review of Biology 69, 327–351.
| The avian spleen: a neglected organ.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M%2Fmt12jsQ%3D%3D&md5=cb9dfa6925f6d30fde1f493edb543756CAS |
Kanner J, Hazan B, Doll L (1988) Catalytic ‘free’ iron ions in muscle foods. Journal of Agricultural and Food Chemistry 36, 412–415.
| Catalytic ‘free’ iron ions in muscle foods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXitVentb8%3D&md5=2f98a415e95cf6207f72e2bef0609d47CAS |
Khalaji S, Zaghari M, Hatami KH, Hedari-Dastjerdi S, Lotfi L, Nazarian H (2011) Black cumin seeds, Artemisia leaves (Artemisia sieberi), and Camellia L. plant extract as phytogenic products in broiler diets and their effects on performance, blood constituents, immunity, and cecal microbial population. Poultry Science 90, 2500–2510.
| Black cumin seeds, Artemisia leaves (Artemisia sieberi), and Camellia L. plant extract as phytogenic products in broiler diets and their effects on performance, blood constituents, immunity, and cecal microbial population.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsV2hs7%2FJ&md5=2453bc3b982e30d423ef56bdbe7c1ba9CAS |
Khatibjoo A, Kermanshahi H, Golian A, Zaghari M (2011) The effect of dietary n-6: n-3 ratio and sex on broiler breeder immunity. Poultry Science 90, 2209–2216.
| The effect of dietary n-6: n-3 ratio and sex on broiler breeder immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlGrsb%2FM&md5=54ef48da206b1a4473ebac0caca66192CAS |
King AJ, Uijttenboogaart TG, Vries AD (1995) α‐Tocopherol, β‐Carotene and Ascorbic Acid as antioxidants in stored poultry muscle. Journal of Food Science 60, 1009–1012.
| α‐Tocopherol, β‐Carotene and Ascorbic Acid as antioxidants in stored poultry muscle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXosVKjtLw%3D&md5=dd8f802df9e4e3654186ae3f628d0474CAS |
Laudadio V, Ceci E, Lastella NM, Tufarelli V (2015) Dietary high-polyphenols extra-virgin olive oil is effective in reducing cholesterol content in eggs. Lipids in Health and Disease 14, 5
| Dietary high-polyphenols extra-virgin olive oil is effective in reducing cholesterol content in eggs.Crossref | GoogleScholarGoogle Scholar |
Lauridsen C (2010) Evaluation of the effect of increasing dietary vitamin E in combination with different fat sources on performance, humoral immune responses and antioxidant status of weaned pigs. Animal Feed Science and Technology 158, 85–94.
| Evaluation of the effect of increasing dietary vitamin E in combination with different fat sources on performance, humoral immune responses and antioxidant status of weaned pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtFant7w%3D&md5=990937ed6bbdb88938d3c05b8ab15fa4CAS |
Lauridsen C, Jensen C, Jakobsen K, Engberg RM, Andersen JO, Jensen SK, Bertelsen G (1997) The influence of vitamin c on the antioxidative status of chickens in vivo at slaughter and on the oxidative stability of broiler meat products. Acta Agriculturae Scandinavica A – Animal Science 47, 187–196.
Leeson S (2007) Vitamin requirements: is there basis for re-evaluating dietary specifications? World’s Poultry Science Journal 63, 255–266.
| Vitamin requirements: is there basis for re-evaluating dietary specifications?Crossref | GoogleScholarGoogle Scholar |
Li SX, Ahn DU, Cherian G, Chung TY, Sim JS (1996) Dietary oils and tocopherol supplementation on cholesterol oxide formation in freeze-dried chicken meat during storage. Journal of Food Lipids 3, 27–42.
| Dietary oils and tocopherol supplementation on cholesterol oxide formation in freeze-dried chicken meat during storage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XksFenu74%3D&md5=f0d6946da875fbca9cd49cd8a64f955dCAS |
Lopez-Ferrer S, Baucells MD, Barroeta AC, Grashorn MA (1999) n-3 enrichment of chicken meat using fish oil: alternative substitution with rapeseed and linseed oils. Poultry Science 78, 356–365.
| n-3 enrichment of chicken meat using fish oil: alternative substitution with rapeseed and linseed oils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvVKqtr0%3D&md5=29449dc0599f6006cbecfd851f3fe4a3CAS |
Manz RA, Hauser AE, Hiepe F, Radbruch A (2005) Maintenance of serum antibody levels. Annual Review of Immunology 23, 367–386.
| Maintenance of serum antibody levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktFOjur0%3D&md5=780a3f2b09b995ce7ccb2147a58cb3d6CAS |
Maraschiello C, Sárraga C, Garcia Regueiro JA (1999) Glutathione peroxidase activity, TBARS, and α-tocopherol in meat from chickens fed different diets. Journal of Agricultural and Food Chemistry 47, 867–872.
| Glutathione peroxidase activity, TBARS, and α-tocopherol in meat from chickens fed different diets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXht12gsLc%3D&md5=560283c6580e1809ac2181d7ed6e9a5aCAS |
Mastrangelo AM, Jeitner TM, Eaton JW (1998) Oleic acid increases cell surface expression and activity of CD11b on human neutrophils. Journal of Immunology (Baltimore, Md.: 1950) 161, 4268–4275.
Morrissey PA, Sheehy PJA, Galvin K, Kerry JP, Buckley DJ (1998) Lipid stability in meat and meat products. Meat Science 49, S73–S86.
| Lipid stability in meat and meat products.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmtFGltLY%3D&md5=d92f0e37129abea7ce5c41a9af30ca27CAS |
Niu ZY, Liu FZ, Yan QL, Li WC (2009) Effects of different levels of vitamin E on growth performance and immune responses of broilers under heat stress. Poultry Science 88, 2101–2107.
| Effects of different levels of vitamin E on growth performance and immune responses of broilers under heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1OgsbjF&md5=e49aaec2f5d3914533c76acb5ed7c9f1CAS |
NRC (National Research Council) (1994) ‘Nutrient requirements of poultry.’ 9th revised edn. (National Academy Press: Washington, DC)
Panda AK, Ramarao SV, Raju MVLN, Chatterjee RN (2008) Effect of dietary supplementation with vitamins E and C on production performance, immune responses and antioxidant status of White Leghorn layers under tropical summer conditions. British Poultry Science 49, 592–599.
| Effect of dietary supplementation with vitamins E and C on production performance, immune responses and antioxidant status of White Leghorn layers under tropical summer conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtF2rsr%2FN&md5=1426062e414c5a039f07ebb6a0e10df8CAS |
Puthpongsiriporn U, Scheideler SE, Sell JL, Beck MM (2001) Effects of vitamin E and C supplementation on performance, in vitro lymphocyte proliferation, and antioxidant status of laying hens during heat stress. Poultry Science 80, 1190–1200.
| Effects of vitamin E and C supplementation on performance, in vitro lymphocyte proliferation, and antioxidant status of laying hens during heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtVylt78%3D&md5=2a14995ccd5e32a8e17dde7028997cc0CAS |
Ross Broilers Manual (2012) ‘Ross 308 broiler nutrition manual.’ (Ross Broiler Ltd: Newbridge, Midlothian, UK)
Ruiz JA, Perez-Vendrell AM, Esteve-Garcia E (1999) Effect of β-carotene and vitamin E on oxidative stability in leg meat of broilers fed different supplemental fats. Journal of Agricultural and Food Chemistry 47, 448–454.
| Effect of β-carotene and vitamin E on oxidative stability in leg meat of broilers fed different supplemental fats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlsVOmtA%3D%3D&md5=8697754696a37757bd50840593caaff3CAS |
SAS Institute (2011) ‘SAS statistics user’s guide. Version 9.3.’ (SAS Institute Inc.: Cary, NC)
Singh H, Sodhi S, Kaur R (2006) Effects of dietary supplements of selenium, vitamin E or combinations of the two on antibody responses of broilers. British Poultry Science 47, 714–719.
| Effects of dietary supplements of selenium, vitamin E or combinations of the two on antibody responses of broilers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitFSksbs%3D&md5=c75cf751b525af6ed90d59791d20854eCAS |
Tengerdy RP, Heinzerling RH, Nockels CF (1972) Effect of vitamin E on the immune response of hypoxic and normal chickens. Infection and Immunity 5, 987–989.
Tufarelli V, Laudadio V (2016) Antioxidant activity of vitamin E and its role in avian reproduction. Journal of Experimental Biology and Agricultural Sciences 4, 266–272.
| Antioxidant activity of vitamin E and its role in avian reproduction.Crossref | GoogleScholarGoogle Scholar |
Tufarelli V, Laudadio V, Casalino E (2016) An extra-virgin olive oil rich in polyphenolic compounds has antioxidant effects in meat-type broiler chickens. Environmental Science and Pollution Research International 23, 6197–6204.
| An extra-virgin olive oil rich in polyphenolic compounds has antioxidant effects in meat-type broiler chickens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvFWhurzE&md5=e489caaff9d5e4892be31baaea8fd531CAS |
Wang A, Xie F, Wang YH, Wu JL (2011) Effects of vitamin C supplementation on growth performance and antioxidant status of layer ducklings. Journal of Animal Physiology and Animal Nutrition 95, 533–539.
| Effects of vitamin C supplementation on growth performance and antioxidant status of layer ducklings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVOntLfM&md5=483c2ef30a5347f99fb55de168580fb2CAS |
Wegmann TG, Smithies O (1966) A simple hemagglutination system requiring small amounts of red cells and antibodies. Transfusion 6, 67–73.
| A simple hemagglutination system requiring small amounts of red cells and antibodies.Crossref | GoogleScholarGoogle Scholar |
Wu CC, Dorairajan T, Lin TL (2000) Effect of ascorbic acid supplementation on the immune response of chickens vaccinated and challenged with infectious bursal disease virus. Veterinary Immunology and Immunopathology 74, 145–152.
| Effect of ascorbic acid supplementation on the immune response of chickens vaccinated and challenged with infectious bursal disease virus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitlKru74%3D&md5=398e3d2a8464232bfe50d2cb7626f0ffCAS |
Zambiazi RC, Przybylski R, Zambiazi MW, Mendonca CB (2007) Fatty acid composition of vegetable oils and fats. Boletim do Centro de Pesquisa de Processamento de Alimentos Curitiba 25, 111–120.
Zhou LJ, Wu H, Li JT, Wang ZY, Zhang LY (2012) Determination of fatty acids in broiler breast meat by near-infrared reflectance spectroscopy. Meat Science 90, 658–664.
| Determination of fatty acids in broiler breast meat by near-infrared reflectance spectroscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvFOisw%3D%3D&md5=7b92b81b10194e54c4cf806b4e225b48CAS |