Duration of the flaxseed diet promotes deposition of n-3 fatty acids in the meat and skin of Peking ducks
Background: Polyunsaturated fatty acids (PUFA), particularly n-3, have beneficial effects on human health, and for this reason foodstuffs with increased content of n-3 PUFA are now very common and widely available.
Design: This study was conducted to investigate the effect of the duration of a flaxseed diet on Peking duck’s growth performance, antioxidant status, gene expression, and fatty acid profile of the meat. A total of 792 12-day-old white Peking ducks were divided into four groups. In the control group, animals were provided with a basal diet. In the three experimental groups, animals were fed a 10% flax seed diet with vitamin E at 13, 23, and 33 days of age for 30, 20, and 10 days, respectively.
Results: The growth performance of the ducks decreased with flaxseed diet’s duration. Both body weight and body weight gain decreased linearly while Feed conversion ratios (FCR) increased in the group of ducks fed flaxseed compared to control ducks. Serum triglycerides (TG), very low density lipoprotein (VLDL), low density lipoprotein cholesterol (LDL-C), and aspartate aminotransferase (AST) linearly decreased while high density lipoprotein cholesterol (HDL-C) and lipopolysaccharide (LPS) levels increased by feeding flaxseed up to 30 days. The expression of lipin-1 gene (LPIN-1) and fatty acid desaturase 2 (FADS2) linearly increased in ducks fed flaxseed for 30 days. Linolenic acid (n-3) and its long-chain metabolites like eicosatetraenoic acid (ETA), eicosapentaenoic acid (EPA), docosahexaenoic acid (DHA), and total n-3 fatty acids (FA) linearly increased while the ratio of n-6 to n-3 was reduced with increased duration of flaxseed supplementation.
Conclusion: Overall, we found that increasing the duration of flaxseed diet with vitamin E for more than 10 days had a mild adverse effect on duck’s growth performance but enrichedits meat with long-chain PUFA and decreased the n-6 to n-3 ratio, providing quality meat for health-conscious consumers. A period of 20 days is good for producing n-3 enriched Peking duck meat and skin.
- Saini RK, Keum YS. Omega-3 and omega-6 polyunsaturated fatty acids: dietary sources, metabolism, and significance – a review. Life Sci 2018; 203: 255–67. doi: 10.1074/jbc.M401231200.
- Desnoyers M, Gilbert K, Rousseau G. Cardioprotective effects of omega-3 polyunsaturated fatty acids: dichotomy between experimental and clinical studies. Marine Drugs 2018; 16: 234. doi: 10.3390/md16070234.
- Nguyen DV, Malau-Aduli BS, Cavalieri J, Nichols PD, Malau-Aduli AE. Supplementation with plant-derived oils rich in omega-3 polyunsaturated fatty acids for lamb production. Vet Anim Sci 2018; 6: 29–40. doi: 10.1016/j.vas.2018.08.001.
- Richieri GV, Ogata RT, Kleinfeld AM. Equilibrium constants for the binding of fatty acids with fatty acid-binding proteins from adipocyte, intestine, heart, and liver measured with the fluorescent probe ADIFAB. J Biol Chem 1994; 269: 23918–30.
- Coe NR, Smith AJ, Frohnert BI, Watkins PA, Bernlohr DA. The fatty acid transport protein (FATP1) is a very long chain acyl-coasynthetase. J Biol Chem 1999; 274: 36300–4. doi: 10.1074/jbc.274.51.36300.
- Chen W, Zhao R, Yan BX, Zhang JS, Huang YQ, Wang ZX, et al. Effects of the replacement of corn oil with linseed oil on fatty acid composition and the expression of lipogenic genes in broiler chickens. Czech J Anim Sci 2014; 59: 353–64. doi: 10.17221/7586-CJAS
- Guillou H, D’Andrea S, Rioux V, Jan S, Legrand P. The surprising diversity of delta 6-desaturase substrates. Biochem Soc Trans 2004; 32: 86–7. doi: 10.1042/BST0320086.
- Kersten S. Integrated physiology and systems biology of PPARα. Mol Metabol 2014; 3: 354–71. doi: 10.1016/j.molmet.2014.02.002.
- Jing M, Gakhar N, Gibson RA, House JD. Dietary and ontogenic regulation of fatty acid desaturase and elongase expression in broiler chickens. Prostaglandins Leukot Essent Fatty Acids 2013; 89: 107–13. doi: 10.1016/j.plefa.2013.05.006.
- Yan BX, Zhao R, Wang JP, ChenW, Huang YQ, Wang ZX, et al. Effect of different dietary oil sources on the growth performance, blood characteristics, fatty acid profiles, and expression of lipogenic genes in the liver of broiler chickens. Czech J Anim Sci 2015; 60: 487–97. doi: 10.17221/8557-CJAS.
- Patsch JR, Prasad S, Gotto JAM, Patsch W. High density lipoprotein2. Relationship of the plasma levels of this lipoprotein species to its composition, to the magnitude of postprandial lipemia, and to the activities of lipoprotein lipase and hepatic lipase. J Clin Invest 1987; 80: 341–7. doi: 10.1172/JCI113078
- Mueller M, Lindner B, Kusumoto S, Fukase K, Schromm AB, Seydel U. Aggregates are the biologically active units of endotoxin. J Biol Chem 2004; 279: 26307–13. doi: 10.1074/jbc.M401231200
- Kaufman RL, Matson CF, Beisel WR.. Hypertriglyceridemia produced by endotoxIn: role of impaired triglyceride disposal mechanisms. J Infect Dis 1976; 133: 548–55. doi: 10.1093/infdis/133.5.548.
- Shim YY, Gui B, Arnison PG, Wang Y, Reaney MJ. Flaxseed (Linum usitatissimum L.) bioactive compounds and peptide nomenclature: a review. Trends Food Sci Technol 2014; 38: 5–20. doi: 10.1016/j.tifs.2014.03.011.
- de-Moura CMA, Junior MSS, Fiorda FA, Caliari M, Vera R, Grossmann MVE. Cooking and texture properties of gluten-free fettuccine processed from defatted flaxseed flour and rice flour. Int J Food Sci Technol 2016; 51: 1495–501. doi: 10.1111/ijfs.13097.
- Parikh M, Maddaford TG, Austria, JA, Aliani M, Netticadan T, Pierce GN. Dietary flaxseed as a strategy or improving human health. Nutrients 2019; 11: 1171. doi: 10.3390/nu11051171
- Priy R, Katoch M, Kumar A, Csk V, Pradesh H, Vishwavidyalya K. Flaxseed-composition and its health benefits. Res Environ Life Sci 2017; 9: 310–16. doi: 10.13140/RG.2.2.35208.93448.
- Mattila PH, Pihlava JM, Hellström J, Nurmi M, Eurola M, Mäkinen, S, et al. Contents of phytochemicals and antinutritional factors in commercial protein-rich plant products. Food Quality Safety 2018; 2: 213–19. doi: 10.1093/fqsafe/fyy021.
- Jankowski J, Zdunczyk Z, Mikulski D, Naczmanski J, Juskiewicz J, Troszynska A, et al. Inclusion of flaxseed in turkey diets decreases the n-6/n-3 PUFA ratio and increases the proportion of biologically active EPA and DHA without affecting meat quality. Eur J Lipid Sci Technol 2015; 117: 797–809. doi: 10.1002/ejlt.201400186.
- Mridula D, Kaur D, Nagra SS, Barnwal P, Gurumayum S, Singh KK. Growth performance and quality characteristics of flaxseed-fed broiler chicks. J Appl Anim Res 2015; 43: 345–51. doi: 10.1080/09712119.2014.978773.
- Salami SA, Majokaa MA, Saha S, Garbera A, Gabarroua JF. Efficacy of dietary antioxidants on broiler oxidative stress, performance and meat quality: science and market. Avian Biol Res 2015; 8 :65–78. doi: 10.3184/175815515X14291701859483.
- Anjum FM, Muhammad FH, Muhammad IK, Muhammad S, Muhammad SA. Impact of extruded flaxseed meal supplemented diet on growth performance, oxidative stability and quality of broiler meat and meat products. Lipids Health Dis 2013; 12: 13. doi: 10.1186/1476-511X-12-13.
- Farag MR, Mahmoud A, Kuldeep D. Flaxseed oil alleviates toxic effects of subacute exposure to acephate on liver and kidney of broiler chicks. Asian J Anim Vet Adv 2017; 12: 61–70. doi: 10.3923/ajava.2017.61.70.
- Barroeta AC. Nutritive value of poultry meat: relationship between vitamin E and PUFA. World Poult Sci J 2007; 63: 277–84. doi: 10.1017/S0043933907001468.
- Leskovec J, Levart A, Nemec Svete A, Peric L, Dukic Stojcic M, Zikic D, et al. Effects of supplementation with α-tocopherol, ascorbic acid, selenium, or their combination in linseed oil-enriched diets on the oxidative status in broilers. Poult Sci 2018; 97: 1641–50. doi: 10.3382/ps/pey004.
- DiNicolantonio JJ, O’Keefe JH. Omega-6 vegetable oils as a driver of coronary heart disease: the oxidized linoleic acid hypothesis. Open Heart 2018; 5:e000898. doi: 10.1136/openhrt-2018-000898
- Huang FR, Zhan ZP, Luo J, Liu ZX, Peng J. Duration of dietary linseed feeding affects the intramuscular fat, muscle mass and fatty acid composition in pig muscle. Livestock Sci 2008; 118: 132–9. doi: 10.1016/j.livsci.2008.01.002.
- Mirshekar R, Boldaji F, Dastar B, Yamchi A, Pashaei S. Longer consumption of flaxseed oil enhances n-3 fatty acid content of chicken meat and expression of FADS2 gene. Eur J Lipid Sci Technol 2015; 117: 810–19. doi: 10.1002/ejlt.201300500.
- The Ministry of Agricultural of the People’s Republic of China. 2004. Chinese performance terms and measurement for poultry (NY/T 823-2004).
- Mikulski D, Jankowski J, Zdunczyk Z, Juskiewicz J, Slominski BA. The effect of different dietary levels of rapeseed meal on growth performance, carcass traits, and meat quality in turkeys. Poult Sci 2012; 91: 215–23. doi: 10.3382/ps.2011-01587.
- Huang L, Ma XY, Jiang ZY, Hu YJ, Zheng CT, Yang XF, et al. Effects of soybean isoflavone on intestinal antioxidant capacity and cytokines in young piglets fed oxidized fish oil. J Zhejiang Univ-Sci B (Biomed & Biotechnol) 2016; 17: 965–74. doi: 10.1631/jzus.B1600078.
- Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative pcr and the 2(-delta deltac (t) method. Methods 2001; 25: 402–8. doi: 10.1006/meth.2001.1262.
- Christie WW. Preparation of ester derivatives of fatty acids for chromatographic analysis. Adv Lipid Methodol 1993; 2: 69–111.
- SPSS Software. SPSS Base 20.0. Chicago, IL: SPSS Inc; 2010.
- National Research Council Subcommittee on Poultry Nutrition. Nutrient requirements of poultry. 9th revised ed. Washington, DC: National Academy Press; 1994. doi: 10.17226/2114.
- Lee SA, Whenham N, Bedford MR. Review on docosahexaenoic acid in poultry and swine nutrition: consequence of enriched animal products on performance and health characteristics. Anim Nutr 2019; 5: 11–21. doi: 10.1016/j.aninu.2018.09.001.
- Neijat M, Ojekudo O, House JD. Effect of flaxseed oil and microalgae DHA on the production performance, fatty acids and total lipids of egg yolk and plasma in laying hens. Prostaglandins Leukot Essent Fatty Acids 2016; 115, 77–88. doi: 10.1016/j.plefa.2016.10.010.
- Wu Y, Wang Y, Yin D, Shahid MS, Yuan J. Flaxseed diet caused inflammation by altering the gut microbiota of Peking ducks. Anim Biotechnol 2019; 30: 1–12. doi: 10.1080/10495398.2019.1634579.
- Klosterman HJ, Lamoureux GL, Parsons JL. Isolation, characterization and synthesis of linatine. A. vitamin B6 antagonist from flaxseed (Linum usitatissimum). Biochemistry 1967; 6: 170–7. doi: 10.1021/bi00853a028.
- Classen HL, Bedford MR. The use of enzymes to improve the nutritive value of poultry feeds. In: Haresign W, Cole DJA, eds. Recent advances in animal nutrition. Oxford, UK: Butterworth-Heinemann LTD; 1991, pp. 95–116.
- Rebole A, Rodriguez ML, Ortiz LT, Alzueta C, Centeno C, Trevino J. Mucilage in linseed: effects on the intestinal viscosity and nutrient digestion in broiler chicks. J Sci Food Agri 2002; 82: 1171–6. doi: 10.1002/jsfa.1164.
- Schwartz RS, Brunzell JD. Increase of adipose tissue lipoprotein lipase activity with weight loss. J Clin Invest 1981; 67: 1425–30. doi: 10.1172/JCI110171
- Fukumitsu S, Aida K, UenoN, Ozawa S, Takahashi Y, Kobori M. Flaxseed lignan attenuates high-fat diet-induced fat accumulation and induces adiponectin expression in mice. Br J Nutr 2008; 100: 669–76. doi: 10.1017/S0007114508911570.
- Wang XK, Chen W, Huang YQ, Kang XT, Wang JP, Li GX, et al. Identification of the transcript isoforms and expression characteristics for chicken Lpin1. Animal 2012; 6: 1897–190. doi: 10.1017/S1751731112001358.
- Du M, Ahn DU. Dietary CLA affects lipid metabolism in broiler chicks. Lipids 2003; 38: 505–11. doi: 10.1007/s11745-003-1091-z.
- Ibrahim D, El-Sayed R, Khater SI, Said EN, El-Mandrawy SAM. Changing dietary n-6:n-3 ratio using different oil sources affects performance, behavior, cytokines mRNA expression and meat fatty acid profile of broiler chickens. Anim Nutri 2017; 4: 44–51. doi: 10.1016/j.aninu.2017.08.003.
- Leaf A, Weber PC. Cardiovascular effects of n-3 fatty acids. N Engl J Med 1988; 318: 549–57. doi: 10.1056/NEJM198803033180905.
- Erridge C, Attina T, Spickett CM, Webb DJ. A high-fat meal induces low grade endotoxemia: evidence of a novel mechanism of postprandial inflammation. Am J Clin Nutr 2007; 86: 1286–92. doi: 10.1093/ajcn/86.5.1286.
- Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet induced obesity and diabetes in mice. Diabetes 2008; 57: 1470–81. doi: 10.2337/db07-1403.
- Caesar R, Fak F, Backhed F. Effects of gut microbiota on obesity and atherosclerosis via modulation of inflammation and lipid metabolism. J Intern Med 2010; 268: 320–8. doi: 10.1111/j.1365-2796.2010.02270.x.
- Birjmohun RS, Van-Leuven SI, Levels JHM, van‘t Veer C, Kuivenhoven JA, Meijers JCM, et al. High-density lipoprotein attenuates inflammation and coagulation response on endotoxin challenge in humans. Arteriosclr Thromb Vasc Biol 2007; 27: 1153–8. doi: 10.1161/ATVBAHA.106.136325.
- Ferrini G, Manzanilla E, Menoyo D, Esteve-Garcia E, Baucells M, Barroeta A. Effects of dietary n-3 fatty acids in fat metabolism and thyroid hormone levels when compared to dietary saturated fatty acids in chickens. Livestock Sci 2010; 131: 287–91. doi: 10.1016/j.livsci.2010.03.017.
- Bensadoun A. Lipoprotein-lipase. Annu Rev Nutr 1991; 11: 217–37. doi: 10.1146/annurev.nu.11.070191.001245.
- Abbasi F, Samadi F, Jafari SM, Ramezanpour S, Shargh MS. Ultrasound-assisted preparation of flaxseed oil nanoemulsions coated with alginate-whey protein for targeted delivery of omega-3 fatty acids into the lower sections of gastrointestinal tract to enrich broiler meat. Ultrason Sonochem 2019; 50: 208–17. doi: 10.1016/j.ultsonch.2018.09.014.
- Jankowski J, Zdunczyk Z, Mikulski D, Juskiewicz J, Naczmanski J, Pomianowski JF, et al. Fatty acid profile, oxidative stability, and sensory properties of breast meat from turkeys fed diets with a different n-6/n-3 PUFA ratio. Eur J Lipid Sci Technol 2012; 114: 1025–35. doi: 10.1002/ejlt.201200003.
- Alvarez M, Diez JA, Lopez-Bote CJ, Gallego M, Bautista JM. Short term modulation of lipogenesis by macronutrients in rainbow trout (Oncorhynchus mykiss) hepatocytes. Br J Nutr 2000; 84: 619–28. doi: 10.1017/S0007114500001951.
- Sealls W, Gonzalez M, Brosnan MJ, Black PN, Dirusso CC. Dietary polyunsaturated fatty acids (C18:2 omega 6 and C18:3 omega 3) do not suppress hepatic lipogenesis. Biochim Biophys Acta 2008; 1781: 406–14. doi: 10.1016/j.bbalip.2008.06.010.
- Lodhi IJ, Wei X, Semenkovich CF. Lipoexpediency: de novo lipogenesis as a metabolic signal transmitter. Trends Endocrinol Metabol 2011; 22: 1–8. doi: 10.1016/j.tem.2010.09.002.
- Donkor J, Sariahmetoglu M, Dewald J, Brindley DN, Reue K. Three mammalian lipins act as phosphatidate phosphatases with distinct tissue expression patterns. J Biol Chem 2007; 282: 3450–7. doi: 10.1074/jbc.M610745200.
- Bionaz M, Chen S, Khan MJ, Loor JJ. Functional role of PPARs in ruminants: potential targets for fine-tuning metabolism during growth and lactation. PPAR Res 2013; 2013: 28. doi: 10.1155/2013/684159.
- Finck BN, Gropler MC, Chen Z, Leone TC, Croce MA, Harris TE, et al. Lipin 1 is an inducible amplifier of the hepatic PGC-1α/PPARα regulatory pathway. Cell Metab 2006; 4: 199–210. doi: 10.1016/j.cmet.2006.08.005.
- Poureslami R, Reas K, Turchini GM, Huyghebaert G, De SS. Effect of diet, sex and age on fatty acid metabolism in broiler chickens: n-3 and n-6 PUFA. Br J Nutr 2010; 104: 189–97. doi: 10.1017/S0007114510000395.
- Candela GC, Lopez LMB, Kohen VL. Importance of a balanced omega6/omega3 ratio for the maintenance of health: nutritional recommendations. Nutr Hosp 2011; 26: 323–329. doi: 10.3305/nh.2011.26.2.5117.
- Suh JM, Zeve D, McKay R, Seo J, Salo Z, Li R, et al. Adipose is a conserved dosage-sensitive antiobesity gene. Cell Metabol 2007; 6: 195–207. doi: 10.1016/j.cmet.2007.08.001.
- Krogdahl A. Digestion and absorption of lipids in poultry. J Nutr 1985; 115: 675–85. doi: 10.1093/jn/115.5.675.
- Richieri GV, Ogata RT, Kleinfeld AM. Fatty acid interactions with native and mutant fatty acid binding protein. Mol Cell Biochem 1999; 192: 77–85. doi: 10.1023/A:1006826405151.
- Phan J, Reue K. Lipin, a lipodystrophy and obesity gene. Cell Metabol 2005; 1: 73–83. doi: 10.1016/j.cmet.2004.12.002.
- Han J, Li L, Wang D, Ma H. (-)-Hydroxycitric acid reduced fat deposition via regulating lipid metabolism-related gene expression in broiler chickens. Lipids Health Dis 2016; 15: 37. doi: 10.1186/s12944-016-0208-5.
- Amiridumari H, Sarir H, Afzali N, Fanimakki O. Effects of milk thistle seed against aflatoxin B1 in broiler model. J Res Med Sci 2013; 18: 786–90.
- Cao FL, Zhang XH, Yu WW, Zhao LG, Wang T. Effect of feeding fermented Ginkgo biloba leaves on growth performance, meat quality, and lipid metabolism in broilers. Poult Sci 2012; 91: 1210–21. doi: 10.3382/ps.2011-01886.
- Huang JF, Huang CC, Lai MK, Lin JH, Lee CH, Wang TY. Effects of dietary fish oil on the contents of eicosapentaenoic acid and docosahexaenoic acid and sensory evaluation of the breast meat in mule ducks. Asian Aust J Anim Sci 2006; 19: 231–5. doi: 10.5713/ajas.2006.231.
- Kobus-Cisowska J, Flaczyk E, Rudzińska M, Kmiecik D. Antioxidant properties of extracts from Ginkgo biloba leaves in meatballs. Meat Sci 2014; 97: 174–80. doi: 10.1016/j.meatsci.2014.01.011.
- Canadian Food Inspection Agency. 2003 Guide to food labelling and advertising. Available from: http://www.inspection.gc.ca/english/fssa/labeti/guide/ch7be.shtml#7 [cited 19 April 2008].
- Bhalerao S, Hegde M, Katyare S, Kadam S. Promotion of omega-3 chicken meat production: an Indian perspective. Worlds Poult Sci J. 2014; 70: 365–74. doi: 10.1017/S0043933914000373.
- Behesti-Moghadam MH, Shehab A, Cherian G. Production performance, quality and lipid composition of eggs from laying hens fed heated flaxseed with carbohydrase enzymes. J Appl Poult Res 2019; 0: 1–9. In press. doi: 10.3382/japr/pfz034.
This work is licensed under a Creative Commons Attribution 4.0 International License
Authors retain copyright of their work, with first publication rights granted to SNF Swedish Nutrition Foundation.