Effect of n-3 fatty acids on immune function in broiler chickens

Poultry Science

Volumn 91, Issue 1, 2012, Pages 74-88

  Al Khalifa, H ^a   Givens, D I ^b   Rymer, C ^b   Yaqoob, P ^b  

^a KUWAIT INSTITUTE FOR SCIENTIFIC RESEARCH   (Kuwait)

^b UNIVERSITY OF READING   (United Kingdom)

Author keywords

Cell proliferation; Fish oil; N 3 fatty acid; Phagocytosis

Indexed keywords

FISH OIL; OMEGA 3 FATTY ACID; UNSATURATED FATTY ACID;

ANIMAL; ANIMAL DISEASE; ARTICLE; BLOOD; BLOOD ANALYSIS; BODY WEIGHT; BURSA FABRICII; CHICKEN; DOSE RESPONSE; DRUG EFFECT; FLOW CYTOMETRY; GAS CHROMATOGRAPHY; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; LEUKOCYTE; LYMPHOCYTE SUBPOPULATION; MALE; METABOLISM; ORGAN SIZE; SPLEEN; THYMUS;

ANIMALS; BLOOD CHEMICAL ANALYSIS; BODY WEIGHT; BURSA OF FABRICIUS; CHICKENS; CHROMATOGRAPHY, GAS; DOSE-RESPONSE RELATIONSHIP, DRUG; FATTY ACIDS, OMEGA-3; FATTY ACIDS, UNSATURATED; FISH OILS; FLOW CYTOMETRY; LEUKOCYTES; LYMPHOCYTE SUBSETS; MALE; ORGAN SIZE; SPLEEN; THYMUS GLAND;

EID: 83755178002     PISSN: 00325791     EISSN: 15253171     Source Type: Journal    
DOI: 10.3382/ps.2011-01693     Document Type: Article

References (103)

1. Adler, H. E., and A. J. DaMassa. 1979. Toxicity of endotoxin to chicks. Avian Dis. 23:174-178.
2. Albers, R., J. Antoine, R. Bourdet-Sicard, P. C. Calder, M. Gleeson, B. Lesourd, S. Samartin, I. R. Sanderson, J. F. Loo, F. W. Vas Dias, and B. Watz. 2005. Markers to measure immunomodulation in human nutrition intervention studies. Br. J. Nutr. 94:452-481.
3. Babu, U. S., P. L. Wiesenfeld, R. B. Raybourne, M. J. Myers, and D. Gaines. 2005. Effect of dietary fishmeal on cell-mediated immune response of laying hens. Int. J. Poult. Sci. 4:652-656.
4. Barber, M. D., K. C. H. Fearon, and J. A. Ross. 2005. Eicosapentaenoic acid modulates the immune response, but has no effect on a mimic of antigen-specific responses. Nutrition 21:588-593.
5. Bou, R., F. Guardiola, A. Tres, A. C. Barroeta, and R. Codony. 2004. Effect of dietary fish oil, alpha-tocopherl acetate, and zinc supplementation on the composition and consumer acceptability of chicken meat. Poult. Sci. 83:282-292.
6. Brenner, R. R. 1984. Effect of unsaturated fatty acids on membrane structure and enzymic kinetics. Prog. Lipid Res. 23:69-96.
7. Calder, P. C. 1996. Immunomodulatory and anti-inflammatory effects of n-3 polyunsaturated fatty acids. Proc. Nutr. Soc. 55:737-774.
8. Calder, P. C. 1997. n-3 polyunsaturated fatty acids and cytokine production in health and disease. Ann. Nutr. Metab. 41:203-234.
9. Calder, P. C. 1998a. Fat chance of immunomodulation. Immunol. Today. 19:244-247.
10. Calder, P. C. 1998b. n-3 Polyunsaturated fatty acids and mononuclear phagocyte function. Pages 1-27 in Medical Fatty Acids in Inflammation. J. Kremer, ed. Birkhauser Verlag, Basel, Switzerland.
11. Calder, P. C. 1999. Dietary fatty acids and the immune system. Lipids 34:S137-140.
12. Calder, P. C. 2002. Dietary modification of inflammation with lipids. Proc. Nutr. Soc. 61:345-358.
13. Calder, P. C. 2005. Polyunsaturated fatty acids and inflammation. Pages 423-427 in Inflammation and Haemostasis. Biochemical Society Transactions. Portland Press, Colchester, UK.
14. Calder, P. C. 2006. n-3 Polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am. J. Clin. Nutr. 83:1505S-1519S.
15. Calder, P. C. 2008. The relationship between the fatty acid composition of immune cells and their function. Prostaglandins Leukot. Essent. Fatty Acids 79:101-108.
16. Calder, P. C., J. A. Bond, D. J. Harvey, S. Gordon, and E. A. Newsholme. 1990. Uptake and incorporation of saturated and unsaturated fatty acids into macrophage lipids and their effect upon macrophage adhesion and phagocytosis. Biochem. J. 269:807-814.
17. Calder, P. C., and G. C. Burdge. 2004. Fatty acids. Pages 1-36 in Bioactive Lipids. A. Nicolaou and G. Kokotos, ed. The Oily Press, Bridgewater, MA.
18. Calder, P. C., and E. A. Newsholme. 1993. Influence of antioxidant vitamins on fatty acid inhibition of lymphocyte proliferation. Biochem. Mol. Biol. Int. 29:175-183.
19. Calder, P. C., P. Yaqoob, F. Thies, F. A. Wallace, and E. A. Miles. 2002. Fatty acids and lymphocyte functions. Br. J. Nutr. c87:S31-S48.
20. Cassity, N. A., K. L. Fritsche, and S. C. Huang. 1990. Effect of various dietary fats on antibody production and lymphocyte proliferation. Ann. Meet. Fed. Am. Soc. Exp. Biol. Fed. Am. Soc. Exp. Biol., Washington, DC.
21. Chen, C. H., J. M. Pickel, J. M. Lahti, and M. D. Cooper. 1991. Surface markers on avian immune cells. Pages 1-22 in Avian Cellular Immunology. CRC Press Inc., Boca Raton, FL.
22. Cheng, P. C., M. L. Dykstra, R. N. Mitchell, and S. K. Pierce. 1999. A role for lipid rafts in B cell antigen receptor signaling and antigen targeting. J. Exp. Med. 190:1549-1560.
23. Chilson, O. P., and A. E. Kelly-Chilson. 1989. Mitogenic lectins bind to the antigen receptor on human lymphocytes. Eur. J. Immunol. 19:389-396.
24. Edwards, H. M., Jr., and J. E. Marion. 1963. Influence of dietary menhaden oil on growth rate and tissue fatty acids of the chick. J. Nutr. 81:123-130.
25. Ellis, N. K., M. R. Young, D. A. Nikcevich, M. Newby, R. Plioplys, and H. T. Wepsic. 1986. Stimulation of prostaglandin-dependent macrophage suppressor cells by the subcutaneous injection of polyunsaturated fatty acids. Cell. Immunol. 102:251-260.
26. Erf, G. F. 1997. Immune System Function and Development in Broilers. Center of Excellence for Poult. Sci., ed. Univ. Arkansas, Fayetteville.
27. Erf, G. F., W. G. Bottje, and T. K. Bersi. 1998. CD4, CD8, and TCR defined T-cell subsets in thymus and spleen of 2- and 7-week-old commercial broiler chickens. Vet. Immunol. Immunopathol. 62:339-348.
28. Ewald, S. J., Y.-Y. Lien, L. Lanqing, and L. W. Johnson. 1996. B-haplotype control of CD4/CD8 subsets and TCR V[beta] usage in chicken T lymphocytes. Vet. Immunol. Immunopathol. 53:285-301.
29. Friedman, A., and D. Sklan. 1995. Effect of dietary fatty acids on antibody production and fatty acid composition of lymphoid organs in broiler chicks. Poult. Sci. 74:1463-1469.
30. Fritsche, K. 2007. Important differences exist in the dose-response relationship between diet and immune cell fatty acids. Lipids 42:961-979.
31. Fritsche, K. L., N. A. Cassity, and S. C. Huang. 1991a. Effect of dietary fat source on antibody production and lymphocyte proliferation in chickens. Poult. Sci. 70:611-617.
32. Fritsche, K. L., and P. V. Johnston. 1990. Effect of dietary omega-3 fatty acids on cell-mediated cytotoxic activity in BALB/c mice. Nutr. Res. 10:577-588.
33. Fritsche, K. L., A. N. Cassity, and S. Hauang. 1991b. Effect of dietary fats on the fatty acid compositions of serum and immune tissues in chickens. Poult. Sci. 70:1213-1222.
34. Fujikawa, M., N. Yamashita, K. Yamazaki, E. Sugiyama, H. Suzuki, and T. Hamazaki. 1992. Eicosapentaeoic acid inhibits antigenpresenting cell function of murine splenocytes. Immunology 75:330-335.
35. Rymer, C., and D. I. Givens. 2006. Effect of species and genotype on the efficiency of enrichment of poultry meat with n-3 polyunsaturated fatty acid. Lipids 41:445-451.
36. Grasman, K. A. 2002. Assessing immunological function in toxicological studies of avian wildlife. Integr. Comp. Biol. 42:34-42.
37. Grimble, R. F., and P. S. Tappia. 1995. Modulatory influence of unsaturated fatty acids on the biology of tumor necrosis factoralpha. Biochem. Soc. Trans. 23:282-287.
38. Gudbjarnason, S., and G. Oskarsdottir. 1977. Modification of fatty acid composition of rat heart lipids by feeding cod liver oil. Biochim. Biophys. Acta 487:10-15.
39. Heerklotz, H. 2002. Triton promotes domain formation in lipid raft mixtures. Biophys. J. 83:2693-2701.
40. Huang, S. C., M. L. Misfeldt, and K. L. Fritsche. 1992. Dietary fat influences Ia antigen expression and immune cell populations in the murine peritoneum and spleen. J. Nutr. 122:1219-1231.
41. Jeffery, N. M., P. Sanderson, E. Sherrington, E. Newsholme, and P. Calder. 1996. The ratio of n-6 to n-3 polyunsaturated fatty acids in the rat diet alters serum lipid levels and lymphocyte functions. Lipids 31:737-745.
42. Kartikasari, L. R., R. J. Hughes, M. S. Geier, M. Makrides, and R. A. Gibson. 2010. Diets high in linoleic acid reduce omega-3 long chain polyunsaturated fatty acids in chicken tissues. Pages 64-67 in Aust. Poult. Sci. Symp. University of Sydney, Australia.
43. Katagiri, Y. U., N. Kiyokawa, and J. Fujimoto. 2001. A role for lipid rafts in immune cell signaling. Microbiol. Immunol. 45:1-8.
44. Kew, S., T. Banerjee, A. M. Minihane, Y. E. Finnegan, C. M. Williams, and P. C. Calder. 2003. Relation between the fatty acid composition of peripheral blood mononuclear cells and measures of immune cell function in healthy, free-living subjects aged 25-72 y. Am. J. Clin. Nutr. 77:1278-1286.
45. Kew, S., M. D. Mesa, S. Tricon, R. Buckley, A. M. Minihane, and P. Yaqoob. 2004. Effects of oils rich in eicosapentaenoic and docosahexaenoic acids on immune cell composition and function in healthy humans. Am. J. Clin. Nutr. 79:674-681.
46. Kim, W., Y.-Y. Fan, R. Barhoumi, R. Smith, D. N. McMurray, and R. S. Chapkin. 2008. n-3 Polyunsaturated fatty acids suppress the localization and activation of signaling proteins at the immunological synapse in murine CD4+ T cells by affecting lipid raftformation. J. Immunol. 181:6236-6243.
47. Klasing, K. C., and D. R. Korver. 1997. Leukocytic cytokines regulate growth rate and composition following activation of the immune system. J. Anim. Sci. 75:58-67.
48. Kogut, M. H., V. K. Lowry, R. B. Moyes, L. L. Bowden, R. Bowden, K. Genovese, and J. R. Deloach. 1998. Lymphokine-augmented activation of avian heterophils. Poult. Sci. 77:964-971.
49. Kogut, M. H., I. Muhammad, H. Q. He, V. Philbin, P. Kaiser, and A. Smith. 2005. Expression and function of Toll-like receptors in chicken heterophils. Dev. Comp. Immunol. 29:791-807.
50. Korver, D. R., and K. C. Klasing. 1997. Dietary fish oil alters specific and inflammatory immune responses in chicks. J. Nutr. 127:2039-2046.
51. Leaf, A., and J. X. Kang. 2001. Omega-3 fatty acids and cardiovascular disease. (World Review of Nutrition and Dietetics, Vol. 89). Pages 161-172 in Nutrition and Fitness 1: Diet, Genes, Physical Activity and Health. A. P. Simopoulos and K. N. Pavlou, ed. S Karger AG, Basel, Switzerland.
52. Leca, G., L. Boumsell, M. Fabbi, E. L. Reinherz, and J. M. Kanellopoulos. 1986. The sheep erythrocyte receptor and both alpha1 and beta chains of the human T-lymphocyte antigen receptor bind the mitogenic lectin (phytohaemagglutinin) from Phaseolus vulgaris. Scand. J. Immunol. 23:535-544.
53. Li, H., Y. Zhang, Z. H. Ning, X. M. Deng, Z. X. Lian, and N. Li. 2008. Effect of selection for phagocytosis in dwarf chickens on immune and reproductive characters. Poult. Sci. 87:41-49.
54. Lokesh, B. R., B. German, and J. E. Kinsella. 1988. Differential effects of docosahexaenoic acid and eicosapentaenoic acid on suppression of lipoxygenase pathway in peritoneal macrophages. Biochim. Biophys. Acta 958:99-107.
55. Lopez-Ferrer, S., M. D. Baucells, A. C. Barroeta, J. Galobart, and M. A. Grashorn. 2001a. n-3 Enrichment of chicken meat. 2. Use of precursors of long-chain polyunsaturated fatty acids: Linseed oil. Poult. Sci. 80:753-761.
56. Lopez-Ferrer, S., M. D. Baucells, A. C. Barroeta, and M. A. Grashorn. 1999. N-3 enrichment of chicken meat using fish oil: Alternative substitution with rapeseed and linseed oils. Poult. Sci. 78:356-365.
57. Lopez-Ferrer, S., M. D. Baucells, A. C. Barroeta, and M. A. Grashorn. 2001b. n-3 Enrichment of chicken meat. 1. Use of very long-chain fatty acids in chicken diets and their influence on meat quality: Fish oil. Poult. Sci. 80:741-752.
58. Mayser, P., H. Grimm, and F. Grimminger. 2002. n-3 Fatty acids in psoriasis. Br. J. Nutr. 87:S77-S82.
59. Meydani, S. N., S. Endres, M. M. Woods, B. R. Goldin, C. Soo, A. Morrill-Labrode, C. A. Dinarello, and S. L. Gorbach. 1991. Oral (n-3) fatty acid supplementation suppresses cytokine production and lymphocyte proliferation: Comparison between young and older women. J. Nutr. 121:547-555.
60. Miles, E. A., T. Banerjee, M. M. Dooper, L. M'Rabet, Y. M. Graus, and P. C. Calder. 2004. The influence of different combinations of gamma-linoleinic acid, stearidonic acid, and EPA on immune function in healthy young male subjects. Br. J. Nutr. 91:893-903.
61. Miles, E. A., and P. C. Calder. 1998. Modulation of immune function by dietary fatty acids. Proc. Nutr. Soc. 57:277-292.
62. Miller, D., and P. Robisch. 1969. Comparative effect of herring, menhaden, and safflower oils on broiler tissues fatty acid composition and flavor. Poult. Sci. 48:2146.
63. Moller, A. P., and J. Erritzoe. 2000. Predation against birds with low immunocompetence. Oecologia 122:500-504.
64. Nassar, B. A., Y. Huang, M. Manku, U. Das, N. Morse, and D. Horrobin. 1986. The influence of dietary manipulation with n-3 and n-6 fatty acids on liver and plasma phospholipid fatty acids in rats. Lipids 21:652-656.
65. Parmentier, H. K., M. B. Kreukniet, B. Goeree, T. F. Davison, S. H. M. Jeurissen, E. G. M. Harmsen, and M. G. B. Nieuwland. 1995. Differences in distribution of lymphocyte antigens in chicken lines divergently selected for antibody responses to sheep red blood cells. Vet. Immunol. Immunopathol. 48:155-168.
66. Parmentier, H. K., M. G. B. Nieuwland, M. W. Barwegen, R. P. Kwakkel, and J. W. Schrama. 1997. Dietary unsaturated fatty acids affect antibody responses and growth of chickens divergently selected for humoral responses to sheep red blood cells. Poult. Sci. 76:1164-1171.
67. Peterson, L. D., N. Jeffery, F. Thies, P. Sanderson, E. Newsholme, and P. Calder. 1998a. Eicosapentaenoic and docosahexaenoic acids alter rat spleen leukocyte fatty acid composition and prostaglandin E2 production, but have different effects on lymphocyte functions and cell-mediated immunity. Lipids 33:171-180.
68. Peterson, L. D., F. Thies, P. Sanderson, E. A. Newsholme, and P. C. Calder. 1998b. Low levels of eicosapentaenoic and docosahexaenoic acids mimic the effects of fish oil upon rat lymphocytes. Life Sci. 62:2209-2217.
69. Phipps, R. P., S. H. Stein, and R. L. Roper. 1991. A new view of prostaglandin regulation of the immune response. Immunol. Today 12:349-352.
70. Pompos, L. J., and K. L. Fritsche. 2002. Antigen-driven murine CD4+ T lymphocyte proliferation and Interleukin-2 production are diminished by dietary (n-3) polyunsaturated fatty acids. J. Nutr. 132:3293-3300.
71. Puthpongsiriporn, U., and S. E. Scheideler. 2005. Effects of dietary ratio of linoleic to linolenic acid on performance, antibody production, and in vitro lymphocyte proliferation in two strains of Leghorn pullet chicks. Poult. Sci. 84:846-857.
72. Ratnayake, W. M. N., R. G. Ackman, and H. W. Hulan. 1986. Effect of redfish meal enriched diets on the taste and n-3 PUFA of 42-day-old broiler chickens. J. Sci. Food Agric. 49:59-74.
73. Reis, L. C., and J. R. Hibbeln. 2006. Cultural symbolism of fish and the psychotropic properties of omega-3 fatty acids. (The emerging role of omega-3 fatty acids in psychiatry). Prostaglandins Leukot. Essent. Fatty Acids 75:227-236.
74. Ross Broilers. 2007. Ross (308) Broiler Management Guide. Aviagen Group, Huntsville, AL.
75. Sanderson, P., P. Yaqoob, and P. C. Calder. 1995. Effects of dietary lipid manipulation upon rat spleen lymphocyte functions and the expression of lymphocyte surface molecules. J. Nutr. Environ. Med. 5:119-132.
76. Schmidt, E. B. 1997. n-3 Fatty acids and the risk of coronary heart disease. DMB Danish Med. Bull. 1997:44.
77. Schroeder, R. J., S. N. Ahmed, Y. Zhu, E. London, and D. A. Brown. 1998. Cholesterol and sphingolipid enhance the Triton X-100 insolubility of glycosylphosphatidylinositol-anchored proteins by promoting the formation of detergent-insoluble ordered membrane domains. J. Biol. Chem. 273:1150-1157.
78. Schwalfenberg, G. 2006. Omega-3 fatty acids: Their beneficial role in cardiovascular health. Can. Fam. Physician 52:734-740.
79. Selvaraj, R. K., and G. Cherian. 2004. Changes in delayed type hypersensitivity, egg antibody content, and immune cell fatty acid composition of layer birds fed conjugated linoleic acid, n-6 or n-3 fatty acids. Can. J. Anim. Sci. 84:221-228.
80. Sijben, J. W. C., H. d. Groot, M. G. B. Nieuwland, J. W. Schrama, and H. K. Parmentier. 2000. Dietary linoleic acid divergently affects immune responsiveness of growing layer hens. Poult. Sci. 79:1106-1115.
81. Sijben, J. W. C., M. G. B. Nieuwland, B. Kemp, H. K. Parmentier, and J. W. Schrama. 2001. Interactions and antigen dependence of dietary n-3 and n-6 polyunsaturated fatty acids on antibody responsiveness in growing layer hens. Poult. Sci. 80:885-893.
82. Simopoulos, A. P. 1994. Is insulin resistance influenced by dietary linoleic acid and trans-fatty acids? Free Radic. Biol. Med. 17:367-372.
83. Smith, K. G., and J. L. Hunt. 2004. On the use of spleen mass as a measure of avian immune system. Oecologia 138:28-31.
84. Stubbs, C. D., and A. D. Smith. 1984. The modification of mammalian membrane polyunsaturation and composition in relation to n-3 Fatty acids and leucocyte function membrane fluidity and function. Biochim. Biophys. Acta 779:89-137.
85. Stulnig, T. M., J. Huber, N. Leitinger, E. Imre, P. Angelisová, P. Nowotny, and W. Waldhausl. 2001. Polyunsaturated eicosapentaenoic acid displaces proteins from membrane rafts by altering raft lipid composition. J. Biol. Chem. 276:37335-37340.
86. Surai, P. F., and N. H. C. Sparks. 2000. Tissue-specific fatty acid and alpha-tocopherol profiles in male chickens depending on dietary tuna oil and vitamin E provision. Poult. Sci. 79:1132-1142.
87. Surette, M. E., M. Edens, F. H. Chilton, and K. M. Tramposch. 2004. Dietary echium oil increases plasma and neutrophil longchain (n-3) fatty acids and lowers serum triacylglycerols in hypertriglyceridemic humans. J. Nutr. 134:1406-1411.
88. Svedova, M., L. Vasko, A. Trebunova, R. Kastel, M. Tuckova, and M. Certik. 2008. Influence of linseed and fish oil on metabolic and immunological indicators of laying hens. Acta Vet. (Brno) 77:39-44.
89. Switzer, K. C., D. N. McMurray, J. S. Morris, and R. S. Chapkin. 2003. (n-3) Polyunsaturated fatty acids promote activation-induced cell death in murine T lymphocytes. J. Nutr. 133:496-503.
90. Thies, F., G. Nebe-Von-Caron, J. R. Powell, P. Yaqoob, E. A. Newsholme, and P. C. Calder. 2001. Dietary supplementation with γ-linolenic acid or fish oil decreases T lymphocyte proliferation in healthy older humans. J. Nutr. 131:1918-1927.
91. Wallace, F. A., E. A. Miles, C. Evans, T. E. Stock, P. Yaqoob, and P. C. Calder. 2001. Dietary fatty acids influence the production of Th1- but not Th2-type cytokines. J. Leukoc. Biol. 69:449-457.
92. Wang, Y. W., A. O. Ajuyah, H. H. Sunwoo, G. Cherian, and J. S. Sim. 2002. Maternal dietary n-3 fatty acids alter the spleen fatty acid composition and bovine serum albumin-induced wing web swelling in broilers. Poult. Sci. 81:1722-1727.
93. Wang, Y. W., C. J. Field, and J. S. Sim. 2000. Dietary polyunsaturated fatty acids alter lymphocyte subset proportion and proliferation, serum immunoglobulin G concentration, and immune tissue development in chicks. Poult. Sci. 79:1741-1748.
94. Yang, Q., and T. M. O'Shea. 2009. Dietary echium oil increases tissue (n-3) long-chain polyunsaturated fatty acids without elevating hepatic lipid concentrations in premature neonatal rats. J. Nutr. 139:1353-1359.
95. Yang, X., Y. Guo, X. He, J. Yuan, Y. Yang, and Z. Wang. 2008. Growth performance and immune responses in chickens after challenge with lipopolysaccharide and modulation by dietary different oils. Animal 2:216-223.
96. Yang, X. J., and Y. Guo. 2006. Modulation of intestinal mucosal immunity by dietary polyunsaturated fatty acids in chickens. Food Agric. Immunol. 17:129-137.
97. Yaqoob, P. 1993. The effects of fatty acids on the composition and functions of lymphocytes. PhD Thesis. Univ. Oxford, Oxford, UK.
98. Yaqoob, P. 2010. Mechanisms underlying the immunomodulatory effects of n-3 PUFA. Proc. Nutr. Soc. 69:311-315.
99. Yaqoob, P., and P. Calder. 1995. Effects of dietary lipid manipulation upon inflammatory mediator production by murine macrophages. Cell. Immunol. 163:120-128.
100. Yaqoob, P., E. A. Newsholme, and P. C. Calder. 1995a. The effect of fatty acids on leucocyte subsets and proliferation in rat whole blood. Nutr. Res. 15:279-287.
101. Yaqoob, P., E. A. Newsholme, and P. C. Calder. 1995b. Influence of cell culture conditions on diet-induced changes in lymphocyte fatty acid composition. Biochim. Biophys. Acta 1255:333-340.
102. Zelenka, J., D. Schneiderova, E. Mrkvicova, and P. Dolezal. 2008. The effect of dietary linseed oils with different fatty acid pattern on the content of fatty acids in chicken meat. Vet. Med. 53:77-85.
103. ZhaoGang, X., G. YuMing, C. ShiYong, and Y. JianMin. 2004. Effect of dietary polyunsaturated fatty acid on antibody production and lymphocyte proliferation in laying hens. Acta Zoonutrimenta Sinica 16:29-35.