Dietary supplementation with DHA-rich microalgae improves performance, serum composition, carcass trait, antioxidant status, and fatty acid profile of broilers

Poultry Science

Volumn 97, Issue 6, 2018, Pages 1881-1890

  Long, S F ^a   Kang, S ^a   Wang, Q Q ^a   Xu, Y T ^a   Pan, L ^a   Hu, J X ^a   Li, M ^a   Piao, X S ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

antioxidant status; broiler; microalgae; n 3 polyunsaturated fatty acids; performance

Indexed keywords

ANTIOXIDANT; DOCOSAHEXAENOIC ACID; OMEGA 3 FATTY ACID;

ANALYSIS; ANIMAL; ANIMAL FOOD; BLOOD; CHEMISTRY; CHICKEN; DIET; DIETARY SUPPLEMENT; DRUG EFFECT; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; MICROALGA; PHYSIOLOGY; RANDOMIZATION; VETERINARY MEDICINE;

ANIMAL FEED; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; ANTIOXIDANTS; CHICKENS; DIET; DIETARY SUPPLEMENTS; DOCOSAHEXAENOIC ACIDS; FATTY ACIDS, OMEGA-3; MALE; MICROALGAE; RANDOM ALLOCATION;

EID: 85048045514     PISSN: 00325791     EISSN: 15253171     Source Type: Journal    
DOI: 10.3382/ps/pey027     Document Type: Article

References (71)

1. Abudabos, A. M., A. B. Okab, R. S. Aljumaah, and E. M. Samara. 2013. Nutritional value of green seaweed (ulva lactuca) for broiler chickens. Ital. J. Anim. Sci. 12:612-620.
2. Adkins, Y., and D. S. Kelley. 2010. Mechanisms underlying the cardioprotective effects of omega-3 polyunsaturated fatty acids. J. Nutr. Biochem. 21:781-792.
3. Alasalvar, C., T. Kda, E. Zubcov, F. Shahidi, and M. Alexis. 2002. Differentiation of cultured and wild sea bass (dicentrarchus labrax): total lipid content, fatty acid and trace mineral composition. Food Chem. 79:145-150.
4. Ali, A., and M. S. Memon. 2008. Incorporation of enteromorpha procera ahlner as nutrition supplement in chick's feed. Int. J. Biol. Biotechnol. 5:211-214.
5. AOAC. 2005. Official Methods of Analysis of AOAC International. 18th Ed. USA.
6. Armin, F., S. Rahimi, A. M. Abkenar, Y. G. Ivari, and H. Ebrahimi. 2015. Effect of Sargassum sp. and Vitamin E on stability of fish oil enriched meat in broiler chickens. Iran. J. Appl. Anim. Sci. 5:385-392.
7. Arterburn, L. M., E. B. Hall, and H. Oken. 2006. Distribution, interconversion, and dose response of n-3 fatty acids in humans. Am. J. Clin. Nutr. 83:1467-1476.
8. Bang, H. O., and J. Dyerberg. 1972. Plasma lipids and lipoproteins in greenlandic west coast eskimos. Acta Med. Scand. 192:85-94.
9. Barclay, W. R., K. M. Meager, and J. R. Abril. 1994. Heterotrophic production of long chain omega-3 fatty acids utilizing algae and algae-like microorganisms. J. Appl. Phycol. 6:123-129.
10. Bernstein, A. M., E. L. Ding, W. C. Willett, and E. B. Rimm. 2011. A meta-analysis shows that docosahexaenoic acid from algal oil reduces serum triglycerides and increases hdl-cholesterol and ldlcholesterol in persons without coronary heart disease. J. Nutr. 142:99-104.
11. Betti, M., B. L. Schneider, W. V. Wismer, V. L. Carney, M. J. Zuidhof, and R. A. Renema. 2009. Omega-3-enriched broiler meat: 2. functional properties, oxidative stability, and consumer acceptance. Poult. Sci. 88:1085-1095.
12. Bharath, N., V. Chinnipreetam, V. R. Reddy, and A. K. Panda. 2017. Effect of omega-3 fatty acids enrichment on performance and carcass traits of broiler chicken. Indian J. Anim. Res. 51:489-494.
13. Bou, R., F. Guardiola, A. Grau, S. Grimpa, A. Manich, A. Barroeta, and R. Codony. 2001. Influence of dietary fat source,-tocopherol, and ascorbic acid supplementation on sensory quality of dark chicken meat. Poult. Sci. 80:800-807.
14. Brown, J. A., and T. R. Cline. 1974. Urea excretion in the pig: an indicator of protein quality and amino acid requirements. J. Nutr. 104:542-545.
15. Burdge, G. 2004.-linolenic acid metabolism in men and women: nutritional and biological implications. Curr. Opin. in Clin. Nutr. Metab. Care. 7:137-144.
16. Burghardt, P. R., E. S. Kemmerer, B. J. Buck, A. J. Osetek, C. Yan, L. G. Koch, S. L. Britton, and S. J. Evans. 2010. Dietary n-3: n-6 fatty acid ratios differentially influence hormonal signature in a rodent model of metabolic syndrome relative to healthy controls. Nutr. Metab. 7:53-59.
17. Cachaldora, P., P. Garcia-Rebollar, C. Alvarez, J. C. De Blas, and J. Mendez. 2008. Effect of type and level of basal fat and level of fish oil supplementation on yolk fat composition and n-3 fatty acids deposition efficiency in laying hens. Anim. Feed Sci. Technol. 141:104-114.
18. Cheng, C. H., T. F. Shen, W. L. Chen, and S. T. Ding. 2005. Effects of dietary algal docosahexaenoic acid oil supplementation on fatty acid deposition and gene expression in laying leghorn hens. J. Agr. Sci. 142:683-690.
19. Colla, L. M., A. L. Muccillo-Baisch, and J. A. V. Costa. 2008. Spirulina platensis effects on the levels of total cholesterol, hdl and triacylglycerols in rabbits fed with a hypercholesterolemic diet. Braz. Arch. Biol. Techn. 51:405-411.
20. De Lange, C. F. M. 2000. Overview of determinants of the nutritional value of feed ingredients. Pp. 17-32 in Feed evaluation principles and practices. P. J. sMoughan, M. W. A. Verstegan, and M. I. Visser-Reyneveld, Eds. Wageningen Press, Netherlands.
21. Delles, R. M., Y. L. Xiong, A. D. True, T. Ao, and K. A. Dawson. 2014. Dietary antioxidant supplementation enhances lipid and protein oxidative stability of chicken broiler meat through promotion of antioxidant enzyme activity. Poult. Sci. 93:1561-1570.
22. Eurostat. 2008. Food: From Farm to Fork Statistics. European Commission (Luxembourg, Office for Official Publications of the European Communities).
23. Garg,M. L., L. G. Wood, H. Singh, and P. J.Moughan. 2006.Means of delivering recommended levels of long chain n-3 polyunsaturated fatty acids in human diets. J. Food Sci. 71:66-71.
24. Gatrell, S. K., T. J. Derksen, E. V. O'Neil, and X. G. Lei. 2017. A new type of defatted green microalgae exerts dose-dependent nutritional, metabolic, and environmental impacts in broiler chicks. J. Appl. Poultry Res. 26:357-366.
25. Givens, D. I., and R. A. Gibbs. 2008. Current intakes of EPA and DHA in European populations and the potential of animalderived foods to increase them: Symposium on 'How can the n-3 content of the diet be improved'. P. Nutr. Soc. 67:273-280.
26. Guschina, I. A., and J. L. Harwood. 2006. Lipids and lipid metabolism in eukaryotic algae. P. Lipid Res. 45:160-186.
27. Hakim, A. R. 2013. The potential of heterotrophic microalgae (Schizochytrium sp.) as a source of DHA. Squalen Bulletin of Marine and Fisheries Postharvest and Biotechnology. 7:29-38.
28. Harinder, G., A. Y. H. Leung, and K. Yok-Lam. 2016. Molecular and cellular mechanisms of myelodysplastic syndrome: implications on targeted therapy. Int. J. Mol. Sci. 17:440-459.
29. Jiang, Z. Y., C. Y. Xu, X. X. Chang, W. W. Li, L. Y. Sun, X. B. Yang, and L. F. Yu. 2013. Fatty liver index correlates with non-alcoholic fatty liver disease, but not with newly diagnosed coronary artery atherosclerotic disease in Chinese patients. BMC gastroenterol. 13:110-115.
30. Kahraman, R., H. Ozpinar, I. Abas, H. C. Kutay, H. Eseceli, and M. A. Grashorn. 2004. Effects of different dietary oil sources on fatty acid composition and malondialdehyde levels of thigh meat in broiler chickens. Archiv Fur Geflugelkunde. 68:77-86.
31. Kessi, F. A. 2016. Evaluation of seaweeds as mineral source in broiler diets (Doctoral dissertation, Sokoine University of Agriculture).
32. Kralik, G., S. Ivankovíc, I. Bogut, and J. Csaṕo. 2004. Effect of dietary supplementation with PUFA n-3 on the lipids composition of chicken meat. Acta Alimentaria. 33:129-139.
33. Limdi, J. K., and G. M. Hyde. 2003. Evaluation of abnormal liver function tests. Postgrad. Med. J. 79:307-312.
34. Lopez-Ferrer, S., M. D. Baucells, A. C. Barroeta, and M. A. Grashorn. 2001a. 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.
35. Lopez-Ferrer, S., M. D. Baucells, A. C. Barroeta, J. Galobart, and M. A. Grashorn. 2001b. N-3 enrichment of chicken meat. 2. use of precursors of long-chain polyunsaturated fatty acids: linseed oil. Poult. Sci. 80:753-761.
36. Lu, T., X. L. Piao, Q. Zhang, D. Wang, X. S. Piao, and S. W. Kim. 2010. Protective effects of Forsythia suspensa extract against oxidative stress induced by diquat in rats. Food Chem. Toxicol. 48:764-770.
37. Marckmann, P., and M. Gronbæk. 1999. Fish consumption and coronary heart disease mortality. A systematic review of prospective cohort studies. Eur. J. Clin. Nutr. 53:585-590.
38. Mariey, Y. A., H. R. Samak, H. A. Abou-Khashba, M. A. M. Sayed, and A. E. Abou-Zeid. 2014. Effect of using Spirulina platensis algae as a feed additive for poultry diets: 2 productive performance of broiler. Egy. Poult. Sci. 34:245-258.
39. Mattson, F. H., and S. M. Grundy. 1985. Comparison of effects of dietary saturated, monounsaturated, and polyunsaturated fatty acids on plasma lipids and lipoproteins in man. J. Lipid Res. 26:194-202.
40. Meynier, A., C. Genot, and G. Gandemer. 1999. Oxidation of muscle phospholipids in relation to their fatty acid composition with emphasis on volatile compounds. J. Sci. Food Agr. 79:797-804.
41. Metayer, S., I. Seiliez, A. Collin, S. Duchene, Y. Mercier, P. A. Geraert, and S. Tesseraud. 2008. Mechanisms through which sulfur amino acids control protein metabolism and oxidative status. J. Nutr. Biochem. 19:207-215.
42. Mooney, J. W., E. M. Hirschler, A. K. Kennedy, A. R. Sams, and M. E. V. Elswyk. 1998. Lipid and flavour quality of stored breast meat from broilers fed marine algae. J. Sci. Food Agr. 78:134-140.
43. Mori, T. A., V. Burke, I. B. Puddey, G. F. Watts, D. N. O'Neal, J. D. Best, and L. J. Beilin. 2000. Purified eicosapentaenoic and docosahexaenoic acids have differential effects on serum lipids and lipoproteins, ldl particle size, glucose, and insulin in mildly hyperlipidemic men. Am. J. Clin. Nutr. 71:1085-1094.
44. NRC. 1994. Nutrient Requirements of Poultry. 9th rev. ed. National Academy Press, Washington, DC.
45. O'Keefe, S. F., F. G. Proudfoot, and R. G. Ackman. 1995. Lipid oxidation in meats of omega-3 fatty-acid enriched broiler chickens. Food Res. Int. 28:417-424.
46. Olson, J. A. 1989. ProVitamin A function of carotenoids: the conversion of beta-carotene into Vitamin A. J. Nutr. 119:105-108.
47. Rasmussen, L. B., B. Kiens, B. K. Pedersen, and E. A. Richter. 1994. Effect of diet and plasma fatty acid composition on immune status in elderly men. Am. J. Clin. Nutr. 59:572-577.
48. Renehan, A. G., M. Tyson, M. Egger, R. F. Heller, and M. Zwahlen. 2008. Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospective observational studies. Lancet. 371:569-578.
49. Ribeiro, T., M. M. Lordelo, S. P. Alves, R. J. Bessa, P. Costa, J. P. Lemos, L. M. A. Ferreira, C. M. G. A. Fontes, and J. A. M. Prates. 2013. Direct supplementation of diet is the most efficient way of enriching broiler meat with n-3 long-chain polyunsaturated fatty acids. Brit. Poult. Sci. 54:753-765.
50. Richard, D., K. Kefi, U. Barbe, P. Bausero, and F. Visioli. 2008. Polyunsaturated fatty acids as antioxidants. Pharmacol. Res. 57:451-455.
51. Roche, H. M., and M. J. Gibney. 2000. Effect of long-chain n-3 polyunsaturated fatty acids on fasting and postprandial triacylglycerol metabolism. Am. J. Clin. Nutr. 71:232-237.
52. Rymer, C., and D. I. Givens. 2005. N-3 fatty acid enrichment of edible tissue of poultry: a review. Lipids. 40:121-130.
53. Rymer, C., R. A. Gibbs, and D. I. Givens. 2010. Comparison of algal and fish sources on the oxidative stability of poultry meat and its enrichment with omega-3 polyunsaturated fatty acids. Poult. Sci. 89:150-159.
54. Sardi, L., G. Martelli, L. Lambertini, P. Parisini, and A. Mordenti. 2006. Effects of a dietary supplement of DHA-rich marine algae on Italian heavy pig production parameters. Livest. Sci. 103:95-103.
55. SAS Institute. 1996. SAS User's Guide: Statistics, Version 7.0. SAS Institute, Cary, NC.
56. Schmitz, G., and J. Ecker. 2008. The opposing effects of n-3 and n-6 fatty acids. Prog. Lipid Res. 47:147-155.
57. Schreiner, M., H. W. Hulan, E. Razzazi-Fazeli, J. Bohm, and R. G. Moreira. 2005. Effect of different sources of dietary omega-3 fatty acids on general performance and fatty acid profiles of thigh, breast, liver and portal blood of broilers. J. Sci. Food Agr. 85:219-226.
58. Singh, R. B., M. A. Niaz, J. P. Sharma, R. Kumar, V. Rastogi, and M. Moshiri. 1997. Randomized, double-blind, placebo-controlled trial of fish oil and mustard oil in patients with suspected acute myocardial infarction: the indian experiment of infarct survival-4. Cardiovasc. Drug. Ther. 11:485-491.
59. Straadt, I. K., M. Rasmussen, H. J. Andersen, and H. C. Bertram. 2007. Aging-induced changes in microstructure and water distribution in fresh and cooked pork in relation to water-holding capacity and cooking loss-a combined confocal laser scanning microscopy (clsm) and low-field nuclear magnetic resonance relaxation study. Meat Sci. 75:687-695.
60. Sturdevant, R. A., M. L. Pearce, and S. Dayton. 1973. Increased prevalence of cholelithiasis in men ingesting a serum-cholesterollowering diet. New Engl. J. Med. 288:24-27.
61. Sugano, M. 1996. Characteristics of fats in Japanese diets and current recommendations. Lipids. 31:283-286.
62. Sukhija, P. S., and D. L. Palmquist. 1988. Rapid method for determination of total fatty acid content and composition of feedstuffs and feces. J. Agr. Food Chem. 36:1202-1206.
63. USDA. 2010. Livestock and Poultry: World Markets and Trade. Available: http://www.fas.usda.gov/psdonline/circulars/livestock poultry.pdf Accessed 4 Oct 2013.
64. Wang, D., X. S. Piao, Z. K. Zeng, T. Lu, Q. Zhang, P. F. Li, L. F. Xue, and S. W. Kim. 2011. Effects of keratinase on performance, nutrient utilization, intestinal morphology, intestinal ecology and inflammatory response of weaned piglets fed diets with different levels of crude protein. Asian-Australas. J. Anim. Sci. 24:1718-1728.
65. Wahbeh, M. I. 1997. Amino acid and fatty acid profiles of four species of macro algae from Aqaba and their suitability for use in fish diets. Aquaculture. 159:101-109.
66. Wood, J. D., M. Enser, A. V. Fisher, G. R. Nute, P. R. Sheard, R. I. Richardson, S. I. Hughes, and F. M. Whittington. 2008. Fat deposition, fatty acid composition and meat quality: a review. Meat Sci. 78:343-358.
67. Zahid, P. B., A. Ali, and M. E. J. Zahid. 2001. Brown seaweed as supplement for broiler feed. Hamdard Medicus. XLIV:98-101.
68. 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. Veterińarń Medićna. 53:743-746.
69. Zhang, Q., X. L. Piao, X. S. Piao, T. Lu, D. Wang, and S. W. Kim. 2011. Preventive effect of Coptis chinensis and berberine on intestinal injury in rats challenged with lipopolysaccharides. Food Chem. Toxicol. 49:61-69.
70. Zhang, W., S. Xiao, H. Samaraweera, E. J. Lee, and D. U. Ahn. 2010. Improving functional value of meat products. Meat Sci. 86:15-31.
71. Zhao, R., and G. X. Shen. 2005. Functional modulation of antioxidant enzymes in vascular endothelial cells by glycated LDL. Atherosclerosis. 179:277-284.