Seamustard (Undaria pinnatifida) Improves Growth, Immunity, Fatty Acid Profile and Reduces Cholesterol in Hanwoo Steers

  • Hwang, J.A. (Department of Animal Science and Technology, Sunchon National University) ;
  • Islam, M.M. (Department of Animal Science and Technology, Sunchon National University) ;
  • Ahmed, S.T. (Department of Animal Science and Technology, Sunchon National University) ;
  • Mun, H.S. (Department of Animal Science and Technology, Sunchon National University) ;
  • Kim, G.M. (Department of Animal Science and Technology, Sunchon National University) ;
  • Kim, Y.J. (Department of Animal Science and Technology, Sunchon National University) ;
  • Yang, C.J. (Department of Animal Science and Technology, Sunchon National University)
  • 투고 : 2014.01.29
  • 심사 : 2014.04.10
  • 발행 : 2014.08.01


The study was designed to evaluate the effect of 2% seamustard (Undaria pinnatifida) by-product (SW) on growth performance, immunity, carcass characteristics, cholesterol content and fatty acid profile in Hanwoo steers. A total of 20 Hanwoo steers (ave. 22 months old; 619 kg body weight) were randomly assigned to control (basal diet) and 2% SW supplemented diet. Dietary SW supplementation significantly (p<0.05) improved average daily gain and gain:feed ratio as well as serum immunoglobulin G concentration. Chemical composition and quality grade of meat and carcass yield grades evaluated at the end of the trial were found to be unaffected by SW supplementation. Dietary SW significantly reduced meat cholesterol concentration (p<0.05). Dietary SW supplementation significantly reduced the myristic acid (C14:0) and palmitoleic acid (C16:ln-7) concentration, while SW increased the concentration of stearic acid (C18:0) and linolenic acid (C18:3n-3) compared to control (p<0.05). Dietary SW supplementation had no effect on saturated fatty acids (SFA), unsaturated fatty acids, poly unsaturated fatty acid (PUFA) or mono unsaturated fatty acid content in muscles. A reduced ratio of PUFA/SFA and n-6/n-3 were found in SW supplemented group (p<0.05). In conclusion, 2% SW supplementation was found to improve growth, immunity and fatty acid profile with significantly reduced cholesterol of beef.


Seaweed;Immunity;Carcass Quality;Cholesterol;Fatty Acid;Hanwoo Steer


  1. Wu, J. and S. Peng. 1997. Comparison of hypolipidemic effect of refined konjac meal with several common dietary fibers and their mechanisms of action. Biomed. Environ. Sci. 10:27-37.
  2. Yang, C. J., I. Y. Yang, D. H. Oh, I. H. Bae, S. G. Cho, I. G. Kong, D. Uuganbayar, I. S. Nou, and K. S. Choi. 2003. Effect of green tea by-product on performance and body composition in broiler chicks. Asian Australas. J. Anim. Sci. 16:867-872.
  3. Zaki, M. A., A. M. Nour, E. Omar, and A. E. Tag El-Din. 1994. The use of seaweed meal in feeding common carp (Cyprinus carpio). Asian Australas. J. Anim. Sci. 7:183-189.
  4. Zalabak, V., J. Kejmar, M. Rosa, and F. Stros. 1990. Algae. In: Nonconventional Feedstuffs in the Nutrition of Farm Animals (Ed. K. Boda). Elsevier, Amsterdam, The Netherlands.
  5. Zerbini, E. and C. E. Polan. 1985. Protein sources evaluated for ruminating Holstein calves. J. Dairy Sci. 68:1416-1424.
  6. Tsuda, K., S. Akagi, and Y. Kishida. 1957. Discovery of cholesterol in some red algae. Science 126(3279):927-928.
  7. Turner, J. L., S. S. Dritz, J. J. Higgins, and J. E. Minton. 2002. Effects of Ascophyllum nodosum extracts on growth performance and immune function of young pigs challenged with Salmonella typhimurium. J. Anim. Sci. 80:1947-1953.
  8. Van Soest, P. J., J. B. Robertson, and B. A. Lewis. 1991. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J. Dairy Sci. 74:3583-3597.
  9. Vasta, V., H. P. S. Makkar, M. Mele, and A. Priolo. 2009. Ruminal biohydrogenation as affected by tannins in vitro. Br. J. Nutr. 102:82-92.
  10. Vasta, V., M. Mele, A. Serra, M. Scerra, G. Luciano, M. Lanza, and A. Priolo. 2009a. Metabolic fate of fatty acids involved in ruminal biohydrogenation in sheep fed concentrate or herbage with or without tannins. J. Anim. Sci. 87:2674-2684.
  11. Volman, J. J., J. D. Ramakers, and J. Plat. 2008. Dietary modulation of immune function by $\beta$-glucans. Physiol. Behav. 94:276-284.
  12. Wang, Y., B. P. Berg, L. R. Barbieri, D. M. Veira, and T. A. McAllister. 2006. Comparison of alfalfa or mixed alfalfasainfoin pastures for grazing cattle: Effects on incidence of bloat, ruminal fermentation, and feed intake. Can. J. Anim. Sci. 86:383-392.
  13. Wang, Y., G. B. Douglas, G. C. Waghorn, T. N. Barry, and A. G. Foote. 1996. The effect of condensed tannins in Lotus corniculatus upon lactation performance in twin-bearing ewes. J. Agric. Sci. (Camb.). 126:353-362.
  14. Waterman, P. G. and S. Mole. 1994. Analysis of phenolic plant metabolites. In: Methods in Ecology. Blackwell Scientific Publications, Oxford, UK.
  15. Sackmann, J. R., S. K. Duckett, M. H. Gillis, C. E. Realini, A. H. Parks, and R. B. Eggelston. 2003. Effects of forage and sunflower oil levels on ruminal biohydrogenation of fatty acids and conjugated linoleic acid formation in beef steers fed finishing diets. J. Anim. Sci. 81:3174-3181.
  16. Saker, K. E., J. H. Fike, H. Veit, and D. L. Ward. 2004. Brown seaweed-(TascoTM) treated conserved forage enhances antioxidant status and immune function in heat-stressed wether lambs. J. Anim. Physiol. Anim. Nutr. 88:122-130.
  17. Saker, K. E., V. G. Allen, J. P. Fontenot, C. P. Bagley, R. L. Ivy, R. R. Evans, and D. B. Wester. 2001. Tasco-Forage: II. Monocyte immune cell response and performance of beef steers grazing tall fescue treated with a seaweed extract. J. Anim. Sci. 79:1022-1031.
  18. SAS Institute Inc. 2003. SAS User's Guide. 9.1 Edition, SAS Institute Inc., Cary, NC, USA.
  19. Sturdivant, C. A, D. K. Lunt, G. C. Smith, and S. B. Smith. 1992. Fatty acid composition of subcutaneous and intramuscular adipose tissues and M. Longissimus dorsi of Wagyu cattle. Meat Sci. 32:449-458.
  20. Swartz, L. A., A. J. Heinrichs, G. A. Varga, and L. D. Muller. 1989. Varying undegradable intake protein on feed intake and growth of dairy calves from birth to 24 weeks of age. J. Dairy Sci. 72(Suppl. 1):529.
  21. Taher, M. 1986. The Use of Marine Seaweed in Broilers Nutrition. M. Sc. Thesis, Alexandria University, Alexandria, Egypt.
  22. Tomlinson, D. J., R. E. James, and M. L. McGilliard. 1989. Effect of TDN and degradable protein on intake, daily gain and subsequent lactation of Holstein heifers. J. Dairy Sci. 72(Suppl. 1):416 (Abstr.)
  23. Tomlinson, D. L., R. E. James, G. L. Bethard, and M. L. McGilliard. 1997. Influence of undegradability of protein in the diet on intake, daily gain, feed efficiency, and body composition of Holstein heifers. J. Dairy Sci. 80:943-948.
  24. Murata, M., K. Ishihara, and H. Saito. 1999. Hepatic fatty acid oxidation enzyme activities are stimulated in rats fed the brown seaweed, Undaria pinnatifida (wakame). J. Nutr. 129:146-151.
  25. Murata, M., Y. Sano, K. Ishihara, and M. Uchida. 2002. Dietary fish oil and Undaria pinnatifida (wakame) synergistically decrease rat serum and liver triacylglycerol. J. Nutr. 132:742-747.
  26. Nakamura, T., K. Nagayama, K. Uchida, and R. Tanaka. 1996. Antioxidant activity of phlorotannins isolated from the brown alga Eisenia bicyclis. Fisheries Sci. 62:923-926.
  27. O'Doherty, J. V., S. Dillon, S. Figat, J. J. Callan, and T. Sweeney. 2010. The effect of lactose inclusion and seaweed extract derived from Laminaria spp. on performance, digestibility of diet components and microbial populations in newly weaned pigs. Anim. Feed Sci. Technol. 157:173-180.
  28. OFSI 2013. Oceans Fisheries Science Institute, Wando-gun, Jeollanam-do, Korea. mode=LSD&mid=sec&sid1=102&oid=003&aid=0005009404 (Korean), (English).
  29. Plaza, M., S. Santoyo, L. Jaime, G. Garcia-Blairsy Reina, M. Herrero, F. Senorans, and E. Ibanez. 2010. Screening for bioactive compounds from algae. J. Pharm. Biomed. Anal. 51:450-455.
  30. Preston, T. R. and M. B. Willis. 1974. Intensive beef production In: 2nd Ed. (Ed. Anonymous). Pergamon Press Ltd., London.
  31. Pulz, O. and W. Gross. 2004. Valuable products from biotechnology of microalgae. Appl. Microbiol. Biotechnol. 65:635-648.
  32. Ragan, M. A. and K. W. Glombitza. 1986. Phlorotannins, brown algal polyphenols. Prog. Phycol. Res. 4:129-241.
  33. Read, S. M., G. Currie, and A. Bacic. 1996. Analysis of the structural heterogeneity of laminarin by electrosprayionisation- mass spectrometry. Carbohydr. Res. 281:187-201.
  34. 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.
  35. McHugh, D. J. 2003. A Guide to the Seaweed Industry. FAO Fish Tech. Pap. Rome, Italy. 441:105.
  36. Melton, S., M. Amiri, G. Davis, and W. Backus. 1982. Flavor and chemical characteristics of ground beef from grass-, foragegrain- and grain-finished steers. J. Anim. Sci. 55:77-87.
  37. Min, B. R., G. T. Attwood, W. C. McNabb, A. L. Molan, and T. N. Barry. 2005. The effect of condensed tannins from Lotus corniculatus on the proteolytic activities and growth of rumen bacteria. Anim. Feed Sci. Technol. 121:45-58.
  38. Min, B. R., T. N. Barry, G. T. Attwood, and W. C. McNabb. 2003. The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperate forages: A review. Anim. Feed Sci. Technol. 106:3-19.
  39. Min, B. R., T. N. Barry, W. C. McNabb, and P. D. Kemp. 1998. Effect of condensed tannins on the production of wool and on its processing characteristics in sheep grazing Lotus corniculatus. Aust. J. Agric. Res. 49:599-606.
  40. Mohammed, A. M., M. Atta, S. A. Babiker, and O. A. El Khidir. 2007. Economic evaluation of beef production from Western Sudan Baggara bulls fattened to different slaughter weights. Sudan Academy of Sciences 1:19-29.
  41. Mosley, E. E., G. L. Powell, M. B. Riley, and T. C. Jenkins. 2002. Microbial biohydrogenation of oleic acid to trans isomers in vitro. J. Lipid Res. 43:290-296.
  42. Mueller-Harvey, I. 2006. Review: Unravelling the conundrum of tannins in animal nutrition and health. J. Sci. Food Agric. 86:2010-2037.
  43. Krakowski, L., J. Krzyzanowski, Z. Wrona, and A. K. Siwicki. 1999. The effect of nonspecific immunostimulation of pregnant mares with 1, 3/1, 6 glucan and levamisole on the immunoglobulins levels in colostrum, selected indices of nonspecific cellular and humoral immunity in foals in neonatal and postnatal period. Vet. Immunol. Immunopathol. 68:1-11.
  44. Krakowski, L., J. Krzyzanowski, Z. Wrona, K. Kostro, and A. K. Siwicki. 2002. The influence of nonspecific immunostimulation of pregnant sows on the immunological value of colostrum. Vet. Immunol. Immunopathol. 87:89-95.
  45. Kromhout, D., A. Menotti, B. Bloemberg, C. Arvanis, H. Blackburn, R. Buzina, A. S. Dontas, F. Fidanza, S. Giampaoli, A. Jansen, M. Karvonen, M. Katan, A. Nissinen, S. Nedeljkovic, J. Pekkanen, M. Pekkanen, S. Punsar, L. Rasanen, B. Simic, and H. Toshima. 1995. Dietary saturated and trans fatty acids and cholesterol and 25-year mortality from coronary heart disease: The seven countries study. Prev. Med. 24:308-315.
  46. Laborde, F. L., I. B. Mandell, J. J. Tosh, J. W. Wilton, and J. G. Buchanan-Smith. 2001. Breed effects on growth performance, carcass characteristics, fatty acid composition and palatability attributes in finishing steers. J. Anim. Sci. 79:355-365.
  47. Le Tutour, B. 1990. Antioxidative activities of algal extracts, synergistic effect with vitamin E. Phytochemistry 29:3759-3765.
  48. Lee, K. N., D. Kritchevsky, and M. W. Pariza. 1994. Conjugated linoleic acid and atherosclerosis in rabbits. Atherosclerosis 108:19-25.
  49. Leonard, S. G., T. Sweeney, B. Bahar, K. M. Pierce, B. P. Lynch, and J. V. O'Doherty. 2010. The effects of maternal dietary supplementation with seaweed extract and fish oil on the humoral immune response and performance of suckling piglets. Livest. Sci. 134:211-214.
  50. Mahan, K. L. and S. Escott-Stump. 2000. Nutrition and diet therapy Krause. McGraw-Hill Interamericana, Madrid, Spain.
  51. KAPE. 2012. The beef carcass grading. Korea Institute for Animal Products Quality Evaluation. system/beef.asp Accessed May 15, 2012.
  52. Kim, K. and C. Kim. 1982. Studies on the manufacture of Underia pinnatifida laver and it's physicochemical properties: 1. Histochemical properties. Korean J. Food Sci. Tech. 14:336-341.
  53. Kim, K. and J. Cheong. 1984. Optimum conditions for extracting alginic acid from Undaria pinatifida and amino acid composition of its extraction residue. Korean J. Food Sci. Tech. 16:336-340.
  54. Kim, K. H., Y. S. Kim, Y. K. Lee, and M. B. Baik. 2000. Postmortem muscle glycolysis and meat quality characteristics of intact male Korean native (Hanwoo) cattle. Meat Sci. 55:47-52.
  55. King, A. J., P. Paniangvait, A. D. Jones, and J. B. German. 1998. Rapid method for quantification of cholesterol in turkey meat and products. J. Food Sci. 63:382-385.
  56. Klopfenstein, T. and F. Goedeken. 1986. Animal protein products: Bypass potential. Feed Management 37:12.
  57. Kolb, N., L. Vallorani, N. Milanovic, and V. Stocchi. 2004. Evaluation of marine algae wakame (Undaria pinnatifida) and kombu (Laminaria digitata japonica) as food supplements. Food Technol. Biotechnol. 42:57-62.
  58. Korean Ministry for Food, Agriculture, Forestry and Fisheries. 2008. Guidelines for the care and use of animals in research. (Korean Ministry for Food, Agriculture, Forestry and Fisheries: Seoul, Korea)
  59. Kouba, M. and J. Mourot. 2011. A review of nutritional effects on fat composition of animal products with special emphasis on n-3 polyunsaturated fatty acids. Biochimie 93:13-17.
  60. Griinari, J. M., B. A. Corl, S. H. Lacy, P. Y. Chouinard, K. V. V. Nurmela, and D. E. Bauman. 2000. Conjugated linoleic acid is synthesized endogenously in lactating dairy cows by $\Delta$9- desaturase. J. Nutr. 130:2285-2291.
  61. Gupta, S. and N. Abu-Ghannam. 2011. Bioactive potential and possible health effects of edible brown seaweeds. Trends Food Sci. Technol. 22:315-326.
  62. Han, S. W. and B. O. Lee. 2010. A Study on the purchasing behaviour of consumers for domestic and imported beef in Korea. J. Agric. Life Sci. 22:73-89.
  63. Harvey, R. W., K. M. Snyder, and J. W. Spears. 1982. Alternative protein sources for growing cattle fed corn silage. Page 17 in North Carolina State Univ. Res. Rep., Raleigh, USA.
  64. Haslam, E. 1989. Plant polyphenols: Vegetable tannins revisited. Cambridge University Press, Cambridge, UK.
  65. Holdt, S. L. and S. Kraan. 2011. Bioactive compounds in seaweed: Functional food applications and legislation. J. Appl. Phycol. 23:543-597.
  66. Hwang, H., T. Chen, R. G. Nines, H. C. Shin, and G. D. Stoner. 2006. Photochemoprevention of UVB-induced skin carcinogenesis in SKH-1 mice by brown algae polyphenols. Int. J. Cancer 119:2742-2749.
  67. Jeremiah, L. 1996. The influence of subcutaneous fat thickness and marbling on beef: Palatability and consumer acceptability. Food Res. Int. 29:513-520.
  68. Jones, W. T. and J. L. Mangan. 1977. Complexes of the condensed tannins of sainfoin (Onobrychis viciifolia Scop.) with fraction 1 leaf protein and with submaxillary-mucoprotein, and their reversal by polyethylene glycol and pH. J. Food Sci. Agric. 28:126-136.
  69. Kandasamy, S., W. Khan, F. Evans, A. T. Critchley, and B. Prithiviraj. 2012. $Tasco^{(R)}$ : A product of Ascophyllum nodosum enhances immune response of Caenorhabditis elegans against Pseudomonas aeruginosa infection. Mar. Drugs 10:84-105.
  70. Cherian, G., R. K. Selvaraj, M. P. Goeger, and P. A. Stitt. 2002. Muscle fatty acid composition and thiobarbituric acid-reactive substances of broilers fed different cultivars of sorghum. Poult. Sci. 81:1415-1420.
  71. Choi, J. H., J. I. Kim, I. S. Kim, and T. H. Yoon. 1991. Studies on anti-aging action of brown algae (Undaria pinnatifida): 1. Dose effect of alginic acid as a modulator of anti-aging action in serum lipids. Korean J. Gerontol. 1:173-178.
  72. Darcy-Vrillon, B. 1993. Nutritional aspects of the developing use of marine macroalgae for the human food industry. Int. J. Food Sci. Nutr. 44:23-35.
  73. Dryden, F. and J. Maechello. 1970. Influence of total lipid and fatty acid composition upon the palatability of three bovine muscles. J. Anim. Sci. 31:36-41.
  74. Dubeski, P. L. 1999. Nutrition and immune function in cattle. In: Proceedings of Western Nutrition Conference, Calgary, AB, Canada. pp. 9-22.
  75. Eaton, S., K. Bartlett, and M. Pourfarzam. 1996. Mammalian mitochondrial beta-oxidation. Biochem. J. 320:345-357.
  76. EI-Deek, A. A., N. S. Isshak, S. Hamdy, N. Badawy, and M. A. Asar. 1985. Performance of two strains of laying hens fed on practical diets containing different levels of seaweed during the rearing and laying stages. Egypt. Poult. Sci. 5:1-11.
  77. Fike, J. H., V. G. Allen, R. E. Schmidt, X. Zhang, J. P. Fontenot, C. P. Bagley, R. L. Ivy, R. R. Evans, R. W. Coelho, and D. B. Wester. 2001. Tasco-forage: I. Influence of a seaweed extract on antioxidant activity in tall fescue and in ruminants. J. Anim. Sci. 79:1011-1021.
  78. Fleurence, J. 1999. Seaweed proteins: Biochemical, nutritional aspects and potential uses. Trends Food Sci. Technol. 10:25-28.
  79. Fung, A., N. Hamid, and J. Lu. 2013. Fucoxanthin content and antioxidant properties of Undaria pinnatifida. Food Chem. 136:1055-1062.
  80. Arnold, T. M. and N. M. Targett. 1998. Quantifying in situ rates of phlorotannin synthesis and polymerization in marine brown algae. J. Chem. Ecol. 24:577-595.
  81. Bach, S. J., Y. Wang, and T. A. McAllister. 2008. Effect of feeding sun-dried seaweed (Ascophyllum nodosum) on fecal shedding of Escherichia coli O157:H7 by feedlot cattle and on growth performance of lambs. Anim. Feed Sci. Technol. 142:17-32.
  82. Banaimoon, S. 1992. Fatty acids in marine macroalgae from Southern Yemen (Hadramout) including occurrence of eicosatetraenoic (20: 4) and eicosapentaenoic (20: 5) acids. Botanica Marina 35:165-168.
  83. Barry, T. N. and W. C. McNabb. 1999. The implications of condensed tannins on the nutritive value of temperate forages fed to ruminants. Br. J. Nutr. 81:263-272.
  84. Bauman, D. E., L. H. Baumgard, B. A. Corl, and J. M. Griinari. 2000. Biosynthesis of conjugated linoleic acid in ruminants. J. Anim. Sci. 77(E-suppl):1-15.
  85. Bessa, R. J. B., S. P. Alves, E. Jeronimo, C. M. Alfaia, J. A. M. Prates, and J. Santos-Silva. 2007. Effect of lipid supplements on ruminal biohydrogenation intermediates and muscle fatty acids in lamb. Eur. J. Lipid Sci. Technol. 109:868-883.
  86. Braden, K. W., J. R. Jr. Blanton, J. L. Montgomery, E. van Santen, V. G. Allen, and M. F. Miller. 2007. Tasco supplementation: Effect on carcass characteristics, sensory attributes and retail display shelf-life. J. Anim. Sci. 85:754-768.
  87. Brown, G. D. and S. Gordon. 2005. Immune recognition of fungal $\beta$-glucans. Cell. Microbiol. 7:471-479.
  88. Cameron, N. and M. Enser. 1991. Fatty acid composition of lipid in Longissimus dorsi muscle of Duroc and British Landrace pigs and its relationship with eating quality. Meat Sci. 29:295-307.
  89. Allen, V., K. Pond, K. Saker, J. P. Fontenot, C. P. Bagley, R. L. Ivy, R. R. Evans, R. E. Schmidt, J. H. Fike, X. Zhang, J. Y. Ayad, C. P. Brown, M. F. Miller, J. L. Montgomery, J. Mahan, D. B. Wester, and C. Melton. 2001. Tasco: Influence of a brown seaweed on antioxidants in forages and livestock-a review. J. Anim. Sci. 79:E21-E31.
  90. Al-Shorepy, S. A., G. A. Alhadrami, and I. A. Jamali. 2001. Effect of feeding diets containing seaweed on weight gain and carcass characteristics of indigenous lambs in the United Arab Emirates. Small Rumin. Res. 41:283-287.
  91. Anderson, M., J. Blanton, J. Gleghorn, S. Kim, and J. Johnson. 2006. Ascophyllum nodosum supplementation strategies that improve overall carcass merit of implanted English crossbred cattle. Asian Australas. J. Anim. Sci. 19:1514-1518.
  92. AOAC. 2000. Official Methods of Analysis. 17th edn. Association of Official Analytical Chemists, Washington, DC, USA.
  93. Applegate, R. D. and P. B. Gray. 1995. Nutritional value of seaweed for ruminants. Rangifer 15:15-28.
  94. Arieli, A., D. Sklan, and G. Kissil. 1993. A note on the nutritive value of Ulva lactuca for ruminants. Anim. Sci. 57:329-331.

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