The Metabolic Effects of Conjugated Linoleic Acids (CLA) in Chickens: A Review

Iranian Journal of Applied Animal Science

مقاله 2، دوره 5، شماره 3، آذر 2015، صفحه 517-528   

نوع مقاله: Review Article

نویسندگان

M. Royan^{* 1}؛ B. Navidshad²

¹Department of Animal Biotechnology, Agricultural Biotechnology Research Institute (ABRI), Rasht, Iran

²Department of Animal Science, University of Mohaghegh Ardabili, Ardabil, Iran

چکیده

Conjugated linoleic acids (CLA) are natural constituents of meat and dairy products from ruminants, originating from bacterial biohydrogenation in the rumen. CLA supplementation increases the health benefits of animal-derived foods. There are inconsistent reports of the effects of dietary CLA on chicken’s performance; however, the majority of previous reports cite anti-lipogenic effects of CLA. Diets could be formulated to increase n-3 fatty acid (FA) concentration in chicken meat by feeding n-3 FAs as a replacement for n-6 FA rich ingredients. Off-flavors and the chances of oxidative deterioration during storage of meat have been attributed to highn-3 FA levels in poultry diets. An approach to increase the n-3 FA content and decrease the n-6/n-3 FAs ratio in meat, using conjugated linoleic acid in diets, has been suggested. This review deals with the main topics of CLA metabolic effects in chickens.

کلیدواژه‌ها

chickens؛ conjugated linoleic acid؛ Gene expression؛ lipid metabolism

مراجع

Adolf R., Duval S. and Emeken E. (2000). Biosynthesis of conjugated linoleic acid in humans. Lipids. 35, 131-135.

Atkinson R.L. (1999). Conjugated linoleic acid for altering body composition and treating obesity. Pp. 348-353 in Advances in Conjugated Linoleic Acid Research. M.P. Yurawecz, M.M. Mossoba, J.K.G. Kramer, M.W. Pariza and G.J. Nelson, Eds. AOCS Press, Champaign, IL, USA.

Aydin R., Pariza M. and Cook M. (2001). Olive oil prevents the adverse effects of dietary conjugated linoleic acid on chick hatchability and egg quality.J. Nutr. 131, 800-806.

Azain M.J., Hausman D.B., Sisk M.B., Flatt W.P. and Jewell D.E. (2000). Dietary conjugated linoleic acid reduces rat adipose tissue cell size rather than cell number. J. Nutr. 130, 1548-1554.

Baddini F.A., Pereira N.F., Da Costa F. and Ribeiro B.G. (2009). Conjugated linoleic acid (CLA): effect modulation of body composition and lipid profile. Nutr. Hospital. 24, 422-428.

Badinga L., Selberg K.T., Dinges A.C., Comer C.W. and Miles R.D. (2003). Dietary conjugated linoleic acid alters hepatic lipid content and fatty acid composition in broiler chickens. Poult. Sci. 82, 111-116.

Banni S. (2002). Conjugated linoleic acid metabolism. Curr. Opinion. Lipidol. 13, 261-266.

Banni S. and Martin J.C. (1998). Conjugated linoleic acid and metabolites. Pp. 261-302 in Trans Fatty Acids in Human Nutrition. W.W. Christie and J. L. Se´ be´ dio, Eds. The Oily Press, Dundee, Scotland.

Bassaganya-Riera J. and Hontecillas R. (2006). CLA and n-3 PUFA differentially modulate clinical activity and colonic PPAR-responsive gene expression in a pig model of experimental IBD. Clin. Nutr. 25, 454-465.

Bassaganya-Riera J., Pogranichniy R.M., Jobgen S.C., Halbur P.G., Yoon K.J., O'Shea M. and Hontecillas R. (2003). Conjugated linoleic acid ameliorates viral infectivity in a pig model of virally induced immunosuppression. J. Nutr. 133, 3204-3214.

Berge G.M., Ruyter B. and Asgard T. (2004). Conjugated linoleic acid in diets for juvenile Atlantic salmon (Salmosalar); effects on fish performance, proximate composition, fatty acid and mineral content. Aquaculture. 237, 365-380.

Bhattacharya A., Banu J., Rahman M., Causey J. and Fernandes G. (2006). Biological effects of conjugated linoleic acids in health and disease. J. Nutr. Biochem. 17, 789-810.

Bolukbasi S.C. (2006). Effect of dietary conjugated linoleic acid (CLA) on broiler performance, serum lipoprotein content, muscle fatty sacid composition and meat quality during refrigerated storage. Br. Poult. Sci. 47, 470-476.

Bretillon L., Chardigny J.M., Gregoire O., Berdeaux O. and Sebedio J.L. (1999). Effects of conjugated linoleic acid isomers on the heatic microsomal desaturation activities in vitro. Lipids. 34, 956-969.

Brodie A.E., Manning V.A., Ferguson K.R., Jewell D.E. and Hu C.Y. (1999). Conjugated linoleic acid inhibits differentiation of pre- and post confluent 3T3-L1 preadipocytes but inhibits cell proliferation only in preconfluent cells. J. Nutr. 129, 602-606.

Brown J.M., Boysen M.S., Jensen S.S., Morrison R.F., Storkson J., Lea-Currie R., Pariza M., Mandrup S. and McIntosh M.K. (2003). Isomer-specific regulation of metabolism and PPARs signaling by CLA in human preadipocytes. J. Lipid. Res. 44, 1287-1300.

Brown J.M., Halvorsen Y.D., Lea-Currie Y.R., Geigerman C. and McIntosh M. (2001). Trans-10, cis-12, but not cis-9, trans-11, conjugated linoleic acid attenuates lipogenesis in primary cultures of stromal vascular cells from human adipose tissue. J. Nutr. 131, 2316-2321.

Bouthegourd J.C., Evans P.C., Gripois D., Tiffon B., Blouguit M.E., Roseau S., Lutton C., Tombe D. and Martin J.C. (2002). A CLA mixture prevents body triglyceride accumulation without affecting energy expenditure in Syrian hamsters. J. Nutr. 132, 2682-2689.

Buccioni A., Antongiovanni M., Mele M., Gualtieri M., Minieri S. and Rapaccini S. (2009). Effect of oleic and conjugated linoleic acid in the diet of broiler chickens on the live growth performances, carcass traits and meat fatty acid profile. Italian J. Anim. Sci. 8, 603-614.

Changhua L., Jindong Y., Defa L., Lidan Z., Shiyan Q. and Jianjun X. (2005). Conjugated linoleic acid attenuates the production and gene expression of proinflammatory cytokines in weaned pigs challenged with lipopolysaccharide. J. Nutr. 135, 239-244.

Chin S.F., Liu W., Storkson J.M., Ha Y.L. and Pariza M.W. (1992). Dietary sources of conjugated dienoic isomers of linoleic acid, a newly recognized class of anticarcinogens. J. Food Comp. Anal. 5, 185-197.

Chin S.F., Storkson J.M., Albright K.J., Cook M.E. and Pariza M.W. (1994). Conjugated linoleic acid is a growth factor for rats as shown by enhanced weight gain and improved feed efficiency. J. Nutr. 124, 2344-2349.

Cho S., Ryua C., Yang J., Mbiriri D.T, Choi C.W., Chae J.I., Kim Y.H., Shim K.S., Kim Y.J. and Choi N.J. (2013). Effect of conjugated linoleic acid feeding on the growth performance and meat fatty acid profiles in broiler: meta-analysis. Asian-Australas J. Anim. Sci. 26, 995-1002.

Choi J.S., Jung M.H., Park H.S. and Song J. (2004). Effect of conjugated linoleic acid isomers on insulin resistance and mRNA levels of genes regulating energy metabolism in high-fat-fed rats. Nutrition. 20, 1008-1017.

Choi Y., Kim Y.C., Han Y.B., Park Y., Pariza M.W. and Ntambi J.M. (2000). The trans-10, cis-12 isomer of conjugated linoleic acid down regulatestearoly-CoA desaturase gene expression in 3T3-L1 adipocytes. J. Nutr. 130, 1920-1924.

Choi Y., Park Y., Storkson J.M., Pariza M.W. and Ntambi J.M. (2002). Inhibition of stearoyl-CoA desaturase activity by the cis-9, trans-11 isomer and the trans-10, cis-12 isomer of conjugated linoleic acid in MDA-MB-231 and MCF-7 human breast cancer cells. Biochem. Biophys. Res. Commun. 294, 785-790.

Clement L., Poirier H., Niot I., Bocher V., Guerre-Millo M., Krief S., Staels B. and Besnard P. (2002). Dietary trans-10, cis-12 conjugated linoleic acid induces hyperinsulinemia and fatty liver in the mouse. J. Lipid. Res. 43, 1400-1409.

Cohen C., Perrault G., Voltz C., Steinberg R. and Soubrié P. (2002). SR141716, a central cannabinoid (CB(1)) receptor antagonist, blocks the motivational and dopamine-releasing effects of nicotine in rats. Behav. Pharmacol. 13, 451-463.

Cook M.E., Jerome D. and Pariza M.W. (2000). Method for selectively altering body fat level, feed efficiency, or weight gain. US Patent.6, 378.

Cook M.E., Miller C.C., Park Y. and Pariza M.W. (1993). Immune modulation by altered nutrient metabolism: nutritional control of immune-induced growth depression. Poult. Sci. 72, 1301-1305.

Corl B.A., Baumgard L.H., Dwyer D.A., Griinari J.M., Phillips B.S. and Bauman D.E. (2001). The role of delta (9)-desaturase in the production of cis-9, trans-11 CLA. J. Nutr. Biochem. 12, 622-630.

Degrace P., Demizieux L., Gresti J., Chardigny J.M., Sébédio J.L. and Clouet P. (2004). Hepatic steatosis is not due to impaired fatty acid oxidation capacities in C57BL/6J mice fed the conjugates trans-10, cis-12-isomer of linoleic acid. J. Nutr. 134, 861-867.

Denli M., Okan F. and Doran F. (2004). Effect of conjugated linoleic acid (CLA) on the performance and serum variables of broiler chickens intoxicated with aflatoxin B₁. South African J. Anim. Sci. 34, 97-103.

Denli M., Okan F., Doran F. and Inal T.C. (2005). Effect of dietary conjugated linoleic acid (CLA) on carcass quality, serum lipid variables and histopathological changes of broiler chickens infected with aflatoxin B₁. South African J. Anim. Sci. 35, 109-116.

DeLany J.P., Blohm F., Truett A.A., Scimeca J.A. and West D.B. (1999). Conjugated linoleic acid rapidly reduces body fat content in mice without affecting energy intake. Am. J. Physiol. 276, 1172-1179.

Du M. and Ahn D.U. (2002). Effect of dietary conjugated linoleic acid on the growth rate of live birds and on the abdominal fat content and quality of broiler meat. Poult. Sci. 81, 428-433.

Du M. and Ahn D.U. (2003). Dietary CLA affects lipid metabolism in broiler chicks. Lipids. 38, 505-511.

Engelke C.F., Siebert B.D., Gregg K., Wright A.D.G. and Vercoe P.E. (2004). Kangaroo adipose tissue has higher concentrations of cis 9, trans 11-conjugated linoleic acid than lamb adipose tissue.J. Anim. Feed. Sci. 13, 689-692.

Evans M., Brown J. and NcIntosh M. (2002). Isomer-specific effects of conjugated linoleic acid (CLA) on adiposity and lipid metabolism. J. Nutr. Biochem. 13, 508-516.

Evans M., Geigerman C., Cook J., Curtis L., Kuebler B. and McIntosh M. (2000). Conjugated linoleic acid suppresses triglyceride accumulation and induces apoptosis in 3T3-L1 preadipocytes. Lipids. 35, 899-910.

Fogerty A.C., Ford G.L. and Svoronos D. (1988). Octadeca-9, 11-dienoic acid in foodstuffs and in the lipids of human blood and breast milk. Nutr. Reports. Int. 38, 937-944.

Fritsche J. and Steinhart C. (1998). Amounts of conjugated linoleic acid (CLA) in German foods and evaluation of daily intake. Zeitschrift Lebensm. Unters. Forsch. 206, 77-82.

Gregoire F.M., Smas C.M. and Sul H.S. (1998). Understanding adipocyte differentiation. Physiol. Rev. 78, 783-809.

Griinari J.M. and Bauman D.E. (1999). Biosynthesis of conjugated linoleic acid and its incorporation into meat and milk in ruminants. Pp. 180-200 in Advances in Conjugated Linoleic Acid Research. M.P. Yurawecz, M.M. Mossoba, J.K.G. Kramer, M.W. Pariza and G.J. Nelson, Eds. AOCS Press, Champaign, IL.

Griinari J.M., Corl B.A., Lacy S.H., Chouinard P.Y., Nurmela K.V. and Bauman D.E. (2000). Conjugated linoleic acid is synthesized endogenously in lactating dairy cows by delta (9)-desaturase. J. Nutr. 130, 2285-2291.

Ha Y.L., Grimm N.K. and Pariza M.W. (1987). Anticarcinogens from fried ground beef: heat-altered derivatives of linoleic acid. Carcinogenesis. 8, 1881-1887.

Hargrave K.M., Azain M.J. and Miner J.L. (2005). Dietary coconut oil increases conjugated linoleic acid-induced body fat loss in mice independent of essential fatty acid deficiency. Biochem. Biophys. Acta. 1737, 52-60.

Herzallah S. (2013). Enrichment of conjugated linoleic acid (CLA) in hen eggs and broiler chickens meat by lactic acid bacteria. Br. Poult. Sci. 54,747-752.

Hotamisligil G.S. and Spiegelman B.M. (1994). Tumor necrosis factor alpha: a key component of the obesity-diabetes link. Diabetes. 43, 1271-1278.

Houseknecht K.L., VandenHeuvel J.P., Moya-Camarena S.Y., Portocarrero C.P., Peck L.W., Nickel K.P. and Belury M.A. (1998). Dietary conjugated linoleic acid normalizes impaired glucose tolerance in the Zucker diabetic fatty fa/fa rat. Biochem. Biophys. Res. Commun. 244, 678-682.

Hur S.J., Yang H.S., Park G.B. and Joo S.T. (2007). Effects of dietary glycine betaine on pork quality in different muscle types. Asian- Australas J. Anim. Sci. 20, 1754-1760.

Inoue N., Nagao K., Hirata J., Wang Y.M. and Yanagita T. (2004). Conjugated linoleic acid prevents the development of essential hypertension in spontaneously hypertensive rats. Biochem. Biophys. Res. Commun. 323, 679-684.

Ip C., Dong Y., Ip M.M., Banni S., Carta G., Angioni E., Murru E., Spada S., Melis M.P. and Saebo A. (2002). Conjugated linoleic acid isomers and mammary cancer prevention. Nutr. Cancer. 43, 52-58.

Javadi M., Math J.H., Everts G.H., Hovenier R., Javadi S., Kappert H. and Beynen A.C. (2007). Effect of dietary conjugated linoleic acid on body composition and energy balance in broiler chickens. Br. J. Nutr. 98, 1152-1158.

Joo S.T., Lee J.I., Ha Y.L. and Park G.B. (2002). Effects of dietary conjugated linoleic acid on fatty acid composition, lipid oxidation, color, and water-holding capacity of pork loin. J. Anim. Sci. 80, 108-112.

Kamphuis M.M., Lejeune M.P., Saris W.H. and Westerterp-Plantenga M.S. (2003a). Effect of conjugated linoleic acid supplementation after weight loss on appetite and food intake in overweight subjects.EuropeanJ. Clin. Nutr. 57, 1268-1274.

Kamphuis M.M., Lejeune M.P., Saris W.H. and Westerterp-Plantenga M.S. (2003b). The effect of conjugated linoleic acid supplementation after weight loss on body weight regain, body composition, and resting metabolic rate in overweight subjects. Int. J. Obesity. Rel. Metab. Disord. 27, 840-847.

Kawahara S., Takenoyama S., Takuma K., Muguruma M. and Yamauchl K. (2009). Effects of dietary supplementation with conjugated linoleic acid on fatty acid composition and lipid oxidation in chicken breast meat. Anim. Sci. J. 80(4), 468-474.

Kelley N.S., Hubbard N.E. and Erickson K.L. (2007). Conjugated linoleic acid isomers and cancer. J. Nutr. 137, 2599-2607.

Kennedy S.R. (2007). Bioactive fatty acids as dietary supplements for farmed fish: effects on growth performance, lipid metabolism, gene expression and immune parameters. Ph D. Thesis. University of Stirling, Scotland.

Kepler C.R., Hirons K.P., McNeill J.J. and Tove S.B. (1966). Intermediates and products of the biohydrogenation of linoleic acid by Butyrinvibriofibrisolvens. J. Biol. Chem. 241, 1350-1354.

Khan S.A. and Vanden Heuvel J.P. (2003). Role of nuclear receptors in the regulation of gene expression by dietary fatty acids: a review. J. Nutr. Biochem. 14, 554-567.

Khanal R.C. and Dhiman T.R. (2004). Biosynthesis of conjugated linoleic acid (CLA): a review. Pakistan J. Nutr. 3, 72-81.

Kim H.Y. (2007). Novel metabolism of docosahexaenoic acid in neural cells. J. Biol. Chem. 282, 18661-18665.

Knekt P., Jarvinen R., Seppanen R., Pukkala E. and Aromaa A. (1996). Intake of dairy products and the risk of breast cancer. Br. J. Cancer. 73, 687-691.

Knight T.W., Knowles S., Death A.F., West J., Agnew M., Morris C.A. and Purchas R.W. (2003). Factors affecting the variation in fatty acid concentrations in lean beef from grass-fed cattle in New Zealand and the implications for human health. New Zealand J. Agric. Res. 46, 83-95.

Kramer J.K.G., Sehat N., Dugan M.E.R., Mossoba M.M., Yurawecz M.P. and Roach J.A.G. (1998). Distributions of conjugated linoleic acid (CLA) isomers in tissue lipid classes of pigs fed a commercial CLA mixture determined by gas chromatography and silver ion-high-performance liquid chromatography.Lipids. 33, 549-558.

Kritchevsky D. (2000). Antimutagenic and some other effects of conjugated linoleic acid. Br. J. Nutr. 83, 459-465.

Larsen T.M., Toubro S., Gudmundsen O. and Astrup A. (2006). Conjugated linoleic acid supplementation for 1 y does not prevent weight or body fat regain. Am. J.Clin. Nutr. 83, 606-612.

Larsson S.C., Bergkvist L. and Wolk A. (2005). High-fat dairy food and conjugated linoleic acid intakes in relation to colorectal cancer incidence in the Swedish Mammography Cohort. Am. J. Clin. Nutr. 82, 894-900.

Leaflet A.S. (2004). Dietary Conjugated Linoleic Acid (CLA) Effects Lipid Metabolism in Broiler Chicks R1934: Iowa State University Animal Industry Report.

Lee K.N., Pariza M.W. and Ntambi J.M. (1998). Conjugated linoleic acid decreases hepatic stearoyl-CoA desaturase mRNA expression.Biochem. Biophys. Res. Com. 248, 817-821.

Lee K.W., Lee H.J., Cho H.Y. and Kim Y.J. (2005). Role of the conjugated linoleic acid in the prevention of cancer. Crit. Rev. Food Sci. Nutr. 45, 135-144.

Lin Y., Kreeft A., Schuurbiers J.A.E. and Draijer R. (2001). Different effects of conjugated linoleic acid isomers on lipoprotein lipase activity in 3T3-L1 adipocytes. J. Nutr. Biochem. 12, 183-189.

Long F.Y., Guo Y.M., Wang Z., Liu D., Zhang B.K. and Yang X. (2011). Conjugated linoleic acids alleviate infectious bursal disease virus-induced immunosuppression in broiler chickens. Poult. Sci. 90, 1926-1933.

Long F.Y.,Yang X., Guo Y.M., Wang Z., Yuan J.M., Zhang B.K. and Liu D. (2012). Conjugated linoleic acids alleviate the immunosuppression of peripheral blood T lymphocytes in broiler chickens exposed to cyclosporin A. Poult. Sci. 91,2431-2437.

Martin J.C., Grégorie S., Siess M.H., Genty M., Chardigny J.M., Berdeaux O., Juanéda P. and Sébédio J.L. (2000). Effects of conjugated linoleic acid isomers on lipid-metabolizing enzymes in male rats. Lipids. 35, 91-98.

Masso-Welch P.A., Zangani D., Ip C., Vaughan M.M., Shoemaker S.F., McGee S.O. and Ip M.M. (2004). Isomers of conjugated linoleic acid differ in their effects on angiogenesis and survival of mouse mammary adipose vasculature. J. Nutr. 134, 299-307.

Masso-Welch P.A., Zangani D., Ip C., Vaughan M.M., Shoemaker S., Ramirez R.A. and Ip M.M. (2002). Inhibition of angiogenesis by the cancer chemopreventive agent conjugated linoleic acid. Cancer. Res. 62, 4383-4389.

McLeod R.S., LeBlanc A.M., Langille M.A., Mitchell P.L. and Currie D.L. (2004). Conjugated linoleic acids, atherosclerosis and hepatic very-low-density lipoprotein metabolism. Am. J. Clin. Nutr. 79, 1169-1174.

Mersmann H.J. (2002). Mechanisms for conjugated linoleic acid-mediated reduction in fat deposition.J. Anim. Sci. 80, 126-134.

Miller C.C., Park Y., Pariza M.W. and Cook M.E. (1994). Feeding conjugated linoleic acid to animals partially overcomes catabolic response due to endotoxin injection. Biochem. Biophys. Res. Commun. 198, 1107-1112.

Mosley E.E., McGuire M.K., Williams J.E. and McGuire M.A. (2006). Cis-9, trans-11 conjugated linoleic acid is synthesized from vaccenic acid in lactating women. J. Nutr. 136, 2297-2301.

Moya-Camarena S.Y., Heuvel J.P.V. and Blanchard S.G. (1999). Conjugated linoleic acid is a potent naturally occurring ligand and activator of PPARα.. J. Lipid. Res. 40, 1426-1433. 

Muller H.L., Kirchgessner M., Roth F.X. and Stangl G.I. (2000). Effect of conjugated linoleic acid on energy metabolism in growing- finishing pigs. J. Anim. Physiol. Anim. Nutr. 83, 85-94.

Muller H.L., Stangl G.I. and Kirchgessner M. (1999). Energy balance of conjugated linoleic acid-treated pigs. J. Anim. Physiol. Anim. Nutr. 81, 150-156.

Nagao K., Inoue N., Wang Y.M., Hirata J., Shimada Y., Nagao T., Matsui T. and Yanagita T. (2003). The 10 trans, 12 cis isomer of conjugated linoleic acid suppresses the development of hypertension in Otsuka Long-Evans Tokushima fatty rats. Biochem. Biophys. Res. Com. 306, 134-138.

Nagao K., Inoue N., Wang Y.M., Shirouchi B. and Yanagita T. (2005). Dietary conjugated linoleic acid alleviates nonalcoholic fatty liver disease in Zucker (fa/fa) rats. J. Nutr. 135, 9-13.

Nagao K., Inoue N., Wang Y.M. and Yanagita T. (2003). Conjugated linoleic acid enhances plasma adiponectin level and alleviates hyperinsulinemia and hypertension in Zucker diabetic fatty (fa/fa) rats. Biochem. Biophys. Res. Commun. 310, 562-566.

Ohnuki K., Haramizu S., Ishihara K. and Fushiki T. (2001). Increased energy metabolism and suppressed body fat accumulation in mice by a low concentration of conjugated linoleic acid. Biosci. Biotechnol. Biochem. 65, 2200-2204.

Pariza M.W., Park Y. and Cook M.E. (2000). Mechanisms of action of conjugated linoleic acid, evidence and speculation. Proc. Soc. Exp. Biol. Med. 223, 8-13.

Pariza M.W., Park Y. and Cook M.E. (2001). The biologically active isomers of conjugated linoleic acid. Prog. Lipid. Res. 40, 283-298.

Pariza M.W. (2004). Perspective on the safety and effectiveness of conjugated linoleic acid. Am. J. Clin. Nutr. 79, 1132-1136.

Pariza M.W. and Hargraves W.A. (1985). A beef-derived mutagenesis modulator inhibits initiation of mouse epidermal tumors by 7, 12- dimethylbenz [a] anthracene. Carcinogenesis. 6, 591-593.

Pariza M.W., Ashoor S.H., Chu F.S. and Lund D.B. (1979). Effects of temperature and time on mutagen formation in pan-fried hamburger. Cancer. Letters. 7, 63-69.

Park Y., Albright K.J., Liu W., Storkson J.M., Cook M.E. and Pariza M.W. (1997). Effect of conjugated linoleic acid on body composition of mice. Lipids. 32, 853-858.

Park Y., Albright K.J., Liu W., Storkson J.M., Lin M.E., Cook M.E. and Pariza M.W. (1999a). Changes in body composition in mice during feeding and withdrawal of conjugated linoleic acid. Lipids. 34, 243-248.

Park Y., Storkson J.M., Albright K.J., Liu W. and Pariza M.W. (1999b). Evidence that the trans-10, cis-12 isomer of conjugated linoleic acid induces body composition changes in mice. Lipids. 34, 235-241.

Park Y., Albright K.J., Storkson J.M., Liu W. and Pariza M.W. (2007). Conjugated linoleic acid (CLA) prevents body fat accumulation and weight gain in an animal model. J. Food. Sci. 72, 612-617.

Park Y. and Pariza M.W. (2007). Mechanisms of body fat modulation by conjugated linoleic acid (CLA). Food Res. Int. 40, 311-323.

Park Y., Storkson J.M., Liu W., Albright K.J., Cook M.E. and Pariza M.W. (2004). Structure-activity relationship of conjugated linoleic acid and its cognates in inhibiting heparin-releasable lipoprotein lipase and glycerol release from fully differentiated 3T3-L1 adipocytes. J. Nutr.Biochem. 15, 561-568.

Peters J.M., Park Y., Gonzalez F.J. and Pariza M.W. (2001). Influence of conjugated linoleic acid on body composition and target gene expression in peroxisome-proliferator-activated receptor α-Null Mice. Biochem. Biophys. Acta. 1533, 233-241.

Peterson D.G., Matitashvili E.A. and Bauman D.E. (2003). Diet-induced milk fat depression in dairy cows results in increased trans-10, cis-12 CLA in milk fat and coordinate suppression of mRNA abundance for mammary enzymes involved in milk fat synthesis. J. Nutr. 133, 3098-3102.

Piperova L.S., Teter B.B., Bruckental I., Sampugna J., Mills S.E., Yurawecz M.P., Fritsche J., Ku K. and Erdman R.A. (2000). Mammary lipogenic enzyme activity, trans fatty acids and conjugated linoleic acids are altered in lactating dairy cows fed a milk fat-depressing diet. J. Nutr. 130, 2568-2574.

Rahman S.M., Wang Y., Yotsumoto H., Cha J., Han S., Inoue S. and Yanagita T. (2001). Effects of conjugated linoleic acid on serum leptin concentration, body-fat accumulation and beta-oxidation of fatty acid in OLETF rats. Nutrition. 17, 385-390.

Royan M., Goh Y.M., Othman F., Sazili A.Q. and Navidshad B. (2011a). Effects of dietary conjugated linoleic acid (CLA), n-3 and n-6 fatty acids on performance and carcass traits of broiler chickens. African J. Biotechnol. 75, 17379-17384.

Royan M., Goh Y.M., Othman F., Sazili A.Q. and Navidshad B. (2011b). Effects of conjugated linoleic acid, fish oil and soybean oil on PPARs (α and γ) mRNA expression in broiler chickens and their relation to body fat deposits. Int. J. Mol. Sci. 12, 8581-8595.

Royan M., Meng G.Y., Othman F., Sazili A.Q. and Hanachi P. (2013). Effects of dietary combination of conjugated linoleic acid with fish oil or soybean oil on fatty acid composition of broiler meat. Arch. Geflugelk. 77, 189-198.

Santora J.E., Palmquist D.L. and Roehriq K.L. (2000). Trans-vaccenic acid is desaturated to conjugated linoleic acid in mice. J. Nutr. 130, 208-215.

Satory D.L. and Smith S.B. (1999). Conjugated acid inhibits proliferation but stimualtes lipid filling of murine 3T3-L1 preadipocytes. J. Nutr. 129, 92-97.

Sell J.L., Jin S. and Jeffrey M. (2001). Metabolizable energy value of conjugated linoleic acid for broiler chicks and laying hens. Poult. Sci. 80, 209-214.

Shin D., Narciso-Gaytán C., Park J.H., Smith S.B., Sánchez-Plata M.X. and Ruiz-Feria C.A. (2011). Dietary combination effects of conjugated linoleic acid and flaxseed or fish oil on the concentration of linoleic and arachidonic acid in poultry meat. Poult. Sci. 90, 1340-1347.

Simon O., Manner K., Schafer K., Sagredos A. and Eder K. (2000). Effects of conjugated linoleic acids on protein to fat proportions, fatty acids, and plasma lipids in broilers. European J. Lipid. Sci. Technol. 102, 402-410.

Simon E., Marcarulla M.T., Fernandez-Quintela. A., Rodriguez V.M. and Portillo M.P. (2005). Body fat-lowering effect of conjugated linoleic acid is not due to increases lipolysis. J. Physiol. Biochem. 61, 363-369.

SirriF., MinelliG., Iaffaldano N., Tallarico N. and Franchini A. (2003). Oxidative stability and quality traits of n-3 PUFA enriched chicken meats. Italian J. Anim. Sci. 2, 450-452.

Song H.J., Sneddon A.A., Barker P.A., Bestwick C., Choe S.N., McClinton S., Grant I., Rotondo D., Heys S.D. and Wahle K.W. (2004). Conjugated linoleic acid inhibits proliferation and modulates protein kinase C isoforms in human prostate cancer cells. Nutr. Cancer. 49, 100-108.

Stangl G.I., Muller H. and Kirchgessner M. (1999). Conjugated linoleic acid effects on circulating hormones, metabolites and lipoproteins, and its proportion in fasting serum and erythrocyte membranes of swine. European J. Nutr. 38, 271-277.

Storkson J.M., Park Y., Cook M.E. and Pariza M.W. (2005). Effects of trans-10, cis-12 conjugated linoleic acid (CLA) and cognates on apolipoprotein B secretion in HepG2 cells. Nutr. Res. 25, 387-399.

Suksombat W., Boonmee T. and Lounglawan P. (2007). Effects of various levels of conjugated linoleic acid supplementation on fatty acid content and carcass composition of broilers.Poult. Sci. 86, 318-324.

Szymczyk B. and Pisulewski P.M. (2003). Effects of dietary conjugated linoleic acid on fatty acid composition and cholesterol content of hen egg yolks. Br. J. Nutr. 90, 93-99.

Szymczyk B., Pisulewski P.M., Szczurek W. and Hancazakowski P. (2001). Effects of conjugated linoleic acid on growth performance, feed conversion efficiency and subsequent carcass quality in broiler chickens. Br. J. Nutr. 85, 465-473.

Takahashi K., Kawamata K., Akiba Y., Iwata T. and Kasai M. (2003). Effect of a mixture of conjugated linoleic acid isomers on growth performance and antibody production in broiler chicks. Br. J. Nutr. 89, 691-694.

Terpstra A.H., Beynen A.C., Everts H., Kocsis S., Katan M.B. and Zock P.L. (2002). The decrease in body fat in mice fed conjugated linoleic acid is die to increases in energy expenditure and energy loss in exreta. J. Nutr. 132, 940-945.

Thiel-Cooper R.L., Parrish F.C., Sparks J.C., Wiegand B.R. and Ewan R.C. (2001). Conjugated linoleic acid changes swine performance and carcass composition. J. Anim. Sci. 79, 1821-182.

Tontonoz P., Hu E., Graves R.A., Budavari A.I. and Spiegalman B.M. (1994). mPPAR-y2, tissue specific regulator of an adipocyte enhancer. Genes. Dev. 8, 1224-1234.

Tsuboyama-Kasaoka N., Takahashi M., Tanemura K., Kim H.J., Tange T., Okuyama H., Kasai M., Ikemoto S. and Ezaki O. (2000). Conjugated linoleic acid supplementation reduces adipose tissue by apoptosis and develops lipodystrophy in mice. Diabetes. 49, 1534-1542.

Turpeinen A.M., Mutanen M., Aro A., Salminen I., Basu S., Palmquist D.L. and Griinari J.M. (2002). Bioconversion of vaccenic acid to conjugated linoleic acid in humans. Am. J. Clin. Nutr. 76, 504-510.

Valeille K., Gripois D., Blouquit M.F., Souidi M., Riottot M., Bouthegourd J.C., Serougne C. and Martin J.C. (2004). Lipid atherogenic risk markers can be more favourably influenced by the cis-9, trans-11-octadecadienoate isomer than a conjugated linoleic acid mixture or fish oil in hamsters. Br. J. Nutr. 91, 191-199.

Wahle K.W J., Heys S.D. and Rotondo D. (2004). Conjugated linoleic acids: are the beneficial or detrimental to health? Prog. Lipid. Res. 43, 553-587.

West D.B., Blohm F.Y., Truett A.A. and DeLany J.P. (2000). Conjugated linoleic acid persistently increases total energy expenditure in AKR/J mice without increasing uncoupling protein gene expression. J. Nutr. 130, 2471-2477.

West D.B., James P.D., Patricia M.C., Fawn B., Alycia A.T. and Joseph S. (1998). Effects of conjugated linoleic acid on body fat and energy metabolism in the mouse. Am. J. Physiol. 275, 667-672.

Williams C.M. (2000). Dietary fatty acids and human health. Ann. Zootech. 49, 165-180.

Xu X., Storkson J., Kim S., Sugimoto K., Park Y. and Pariza M.W. (2003). Short-term intake of conjugated linoleic acid inhibits lipoprotein lipase and glucose metabolism but does not enhance lipolysis in mouse adipose tissue. J. Nutr. 133, 663-667.

Yamasaki M., Ikeda A., Hirao A., Tanaka Y., Miyazaki Y., Rikimaru T., Shimada M., Sugimachi K., Tachibana H. and Yamada K. (2001). Effect of dietary conjugated linoleic acid on the in vivo growth of rat heptatoma dRLh-84. Nutr. Cancer. 40, 140-148.

Yanagita T., Wang Y.M., Nagao K., Ujino Y. and Inoue N. (2005). Conjugated linoleic acid-induced fatty liver can be attenuated by combination with docosahexaenoic acid in C57BL/6N mice. J. Agric. Food Chem. 53, 9629-9633.

Zanini S.F., Colnago G.L., Pessotti B.M.S., Bastos M.R., Casagrande F.P. and Lima V.R. (2006). Body fat of broiler chickens fed diets with two fat sources and conjugated linoleic acid. Int. J. Poult. Sci. 5, 241-246.

Zanini S.F., Vicente E., Colnago G.L., Pessotti B.M.S. and Silva M.A. (2008). Manipulation of the fatty acids composition of poultry meat and giblets by dietary inclusion of two oil sources and conjugated linoleic acid. Arquivo Brasileiro de. Med. Vet. Zootec. 60, 1388-1398.

Zhang H., Guo Y. and Yuan J. (2005). Conjugated linoleic acid enhanced the immune function in broiler chicks. Br. J. Nutr. 94, 746-752.