Abstract
The limited efficiency with which dietary alpha-linolenic acid (ALA) is converted by hens into docosahexaenoic acid (DHA) for egg deposition is not clearly understood. In this study, dietary ALA levels were increased via the inclusion of hempseed (HS) and hempseed oil (HO) in hen diets, with the goal of assessing the effects on the fatty acid (FA) profiles of total lipids and lipid classes in yolk, liver and plasma. Forty-eight hens were individually caged and fed one of six diets containing either HS:10, 20 or 30, HO:4.5 or 9.0 (%, diet) or a control (containing corn oil), providing a range (0.1–1.28 %, diet) of ALA. Fatty acid methyl esters of total lipids and lipid classes, including phosphatidyl choline (PtdCho) and ethanolamine (PtdEtn) in yolk, plasma and liver were then determined. Levels of n-3 FAs in both total lipids and lipid classes increased in all tissues. ALA and eicosapentaenoic acid (EPA) increased linearly, while docosapentaenoic acid and DHA increased quadratically. The FA profiles of yolk closely reflected levels in both plasma and liver. While ALA was highly concentrated in the triacylglycerol, it was low but equally distributed between PtdCho and PtdEtn in all tissues; however, the net accumulation was lower (P < 0.0001) in liver compared to yolk and plasma. Levels of EPA and ALA in yolk-PtdEtn were linearly (P < 0.0001; R 2 = 0.93) associated, and reflected those in liver-PtdEtn (P < 0.0001; R 2 = 0.90). In the liver, a strong inverse correlation (P < 0.0001; r = −0.94) between PL-DHA and ALA-to-EPA ratio in PtdEtn supports theories of low substrate availability, possibly limiting the conversion of ALA into DHA for egg enrichment.
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Abbreviations
- ALA:
-
Alpha-Linolenic (18:3n-3)
- ARA:
-
Arachidonic acid (20:4n-6)
- CE:
-
Cholesteryl ester
- DHA:
-
Docosahexaenoic acid (22:6n-3)
- DPA:
-
Docosapentaenoic acid (22:5n-3)
References
Institute of Medicine (2005) Dietary reference intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein, and amino acids. National Academies Press, Washington
Flock MR, Harris WS, Kris-Etherton PM (2013) Long-chain omega-3 fatty acids: time to establish a dietary reference intake. Nutr Rev 71(10):692–707
Fraeye I, Bruneel C, Lemahieu C, Buyse J, Muylaert K, Foubert I (2012) Dietary enrichment of eggs with omega-3 fatty acids: a review. Food Res Int 48(2):961–969
Yashodhara BM, Umakanth S, Pappachan JM, Bhat SK, Kamath R, Choo BH (2009) Omega-3 fatty acids: a comprehensive review of their role in health and disease. Postgrad Med J 85(1000):84–90
González-Esquerra R, Leeson S (2001) Alternatives for enrichment of eggs and chicken meat with omega-3 fatty acids. Can J Anim Sci 81(3):295–305
Cherian G, Sim JS (1991) Effect of feeding full fat flax and canola seeds to laying hens on the fatty acid composition of eggs, embryos, and newly hatched chicks. Poult Sci 70(4):917–922
Scheideler SE, Froning GW (1996) The combined influence of dietary flaxseed variety, level, form, and storage conditions on egg production and composition among vitamin E-supplemented hens. Poult Sci 75(10):1221–1226
Lewis NM, Seburg S, Flanagan NL (2000) Enriched eggs as a source of N-3 polyunsaturated fatty acids for humans. Poult Sci 79(7):971–974
Hargis BM, Van Elswyk ME, Hargis PS (1991) Dietary modification of yolk lipid with menhaden oil. Poult Sci 70(4):874–883
Herber SM, Van Elswyk ME (1996) Dietary marine algae promotes efficient deposition of n-3 fatty acids for the production of enriched shell eggs. Poult Sci 75(12):1501–1507
Harel M, Koven W, Lein I, Bar Y, Behrens P, Stubblefield J, Zohar Y, Place AR (2002) Advanced DHA, EPA and ARA enrichment materials for marine aquaculture using single cell heterotrophs. Aquaculture 213(1–4):347–362
Lawlor JB, Gaudette N, Dickson T, House JD (2010) Fatty acid profile and sensory characteristics of table eggs from laying hens fed diets containing microencapsulated fish oil. Anim Feed Sci Technol 156(3–4):97–103
Lemahieu C, Bruneel C, Termote-Verhalle R, Muylaert K, Buyse J, Foubert I (2013) Impact of feed supplementation with different omega-3 rich microalgae species on enrichment of eggs of laying hens. Food Chem 141(4):4051–4059
Gakhar N, Goldberg E, Jing M, Gibson R, House JD (2012) Effect of feeding hemp seed and hemp seed oil on laying hen performance and egg yolk fatty acid content: evidence of their safety and efficacy for laying hen diets. Poult Sci 91(3):701–711
Callaway JC (2004) Hempseed as a nutritional resource: an overview. Euphytica 140(1–2):65–72
Neijat M, Suh M, Neufeld J, House JD (2015) Hempseed products fed to hens effectively increased n-3 polyunsaturated fatty acids in total lipids, triacylglycerol and phospholipid of egg yolk. Lipids 1–14. doi:10.1007/s11745-015-4088-7
Goldberg EM, Gakhar N, Ryland D, Aliani M, Gibson RA, House JD (2012) Fatty acid profile and sensory characteristics of table eggs from laying hens fed hempseed and hempseed oil. J Food Sci 77(4):S153–S160
Sprecher H (2000) Metabolism of highly unsaturated n-3 and n-6 fatty acids. Biochim Biophys Acta—Mol Cell Biol Lipids 1486(2–3):219–231
Tu WC, Cook-Johnson RJ, James MJ, Mühlhäusler BS, Gibson RA (2010) Omega-3 long chain fatty acid synthesis is regulated more by substrate levels than gene expression. Prostaglandins Leukot Essent Fatty Acids 83(2):61–68
Neijat M, Gakhar N, Neufeld J, House JD (2014) Performance, egg quality, and blood plasma chemistry of laying hens fed hempseed and hempseed oil. Poult Sci 93(11):2827–2840
Olfert ED, Cross BM, McWilliam AA (eds) (1993) Canadian council on animal care. Guide to the care and use of experimental animals, 2nd edn. CCAC, Ottawa
Petrović M, Debeljak Ž, Kezić N, Džidara P (2015) Relationship between cannabinoids content and composition of fatty acids in hempseed oils. Food Chem 170:218–225
Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226(1):497–509
Burdge GC, Wright P, Jones AE, Wootton SA (2000) A method for separation of phosphatidylcholine, triacylglycerol, non-esterified fatty acids and cholesterol esters from plasma by solid-phase extracti on. Br J Nutr 84(5):781–787
Suh M, Wierzbicki AA, Clandinin MT (1994) Dietary fat alters membrane composition in rod outer segments in normal and diabetic rats: impact on content of very-long-chain (C ≥ 24) polyenoic fatty acids. Biochim Biophys Acta—Lipids Lipid Metab 1214(1):54–62
L Hartman (1973) Rapid preparation of fatty acid methyl esters from lipids. LAB.PRACT. vol 22, no 7, pp 475–476
Garg ML, Sebokova E, Wierzbicki A, Thomson ABR, Clandinin MT (1988) Differential effects of dietary linoleic and α-linolenic acid on lipid metabolism in rat tissues. Lipids 23(9):847–852
Portolesi R, Powell BC, Gibson RA (2007) Competition between 24:5n-3 and ALA for Delta 6 desaturase may limit the accumulation of DHA in HepG2 cell membranes. J Lipid Res 48(7):1592–1598
Pita MCG, de Carvalh PR, Reis P, Neto PE, de Mendonc CX Jr (2011) Modulation of plasma levels and percentages of incorporation of ω-3 PUFAs in egg yolk under the influence of supplementation sources rich in omega 3 to diet of laying hens. Pak J Nutr 10(8):735–754
Leskanich CO, Noble RC (1997) Manipulation of the n-3 polyunsaturated fatty acid composition of avian eggs and meat. Worlds Poult Sci J 53(2):176–183
Ivy CA, Nesheim MC (1973) Factors influencing the liver fat content of laying hens. Poult Sci 52(1):281–291
McIndoe WC (1971) Yolk synthesis. In: Bell DJ, Freeman BM (eds) Physiology and biochemistry of the domestic fowl, 3rd edn. Academic Press, London, pp 1209–1223
Evans RJ, Flegal CJ, Foerder CA, Bauer DH, LaVigne M (1977) The influence of crude cottonseed oil in the feed on the blood and egg yolk lipoproteins of laying hens. Poult Sci 56(2):468–479
Palmquist DL (2009) Omega-3 fatty acids in metabolism, health, and nutrition and for modified animal product foods. Prof Anim Sci 25(3):207–249
Rymer C, Givens DI (2005) n-3 Fatty acid enrichment of edible tissue of poultry: a review. Lipids 40(2):121–130
Goyens PLL, Spilker ME, Zock PL, Katan MB, Mensink RP (2005) Compartmental modeling to quantify alpha-linolenic acid conversion after longer term intake of multiple tracer boluses. J Lipid Res 46(7):1474–1483
Jiang Z, Ahn DU, Sim JS (1991) Effects of feeding flax and two types of sunflower seeds on fatty acid compositions of yolk lipid classes. Poult Sci 70(12):2467–2475
Surai PF, Speake BK, Noble RC, Mezes M (1999) Species-specific differences in the fatty acid profiles of the lipids of the yolk and of the liver of the chick. J Sci Food Agric 79(5):733–736
Fredriksson S, Elwinger K, Pickova J (2006) Fatty acid and carotenoid composition of egg yolk as an effect of microalgae addition to feed formula for laying hens. Food Chem 99(3):530–537
Leveille GA, Romsos DR, Yeh Y, O’Hea EK (1975) Lipid biosynthesis in the chick. A consideration of site of synthesis, influence of diet and possible regulatory mechanisms. Poult Sci 54(4):1075–1093
Patel MS, Owen OE, Goldman LI, Hanson RW (1975) Fatty acid synthesis by human adipose tissue. Metabolism 24(2):161–173
Dircks L, Sul HS (1999) Acyltransferases of de novo glycerophospholipid biosynthesis. Prog Lipid Res 38(5–6):461–479
Berge R, Madsen L, Vaagenes H, Tronstad K, Gottlicher M, Rustan A (1999) In contrast with docosahexaenoic acid, eicosapentaenoic acid and hypolipidaemic derivatives decrease hepatic synthesis and secretion of triacylglycerol by decreased diacylglycerol acyltransferase activity and stimulation of fatty acid oxidation. Biochem J 343(1):191–197
Tapiero H, Ba GN, Couvreur P, Tew KD (2002) Polyunsaturated fatty acids (PUFA) and eicosanoids in human health and pathologies. Biomed Pharmacother 56(5):215–222
Salem N Jr, Litman B, Kim HY, Gawrisch K (2001) Mechanisms of action of docosahexaenoic acid in the nervous system. Lipids 36(9):945–959
Madsen L, Rustan AC, Vaagenes H, Berge K, Dyrøy E, Berge RK (1999) Eicosapentaenoic and docosahexaenoic acid affect mitochondrial and peroxisomal fatty acid oxidation in relation to substrate preference. Lipids 34(9):951–963
Coleman DP, Lee R (2004) Enzymes of triacylglycerol synthesis and their regulation. Prog Lipid Res 43(2):134–176
Jump DB (2008) N-3 polyunsaturated fatty acid regulation of hepatic gene transcription. Curr Opin Lipidol 19(3):242–247
Barceló-Coblijn G, Murphy EJ (2009) Alpha-linolenic acid and its conversion to longer chain n-3 fatty acids: benefits for human health and a role in maintaining tissue n-3 fatty acid levels. Prog Lipid Res 48(6):355–374
Liu X, Xue Y, Liu C, Lou Q, Wang J, Yanagita T, Xue C, Wang Y (2013) Eicosapentaenoic acid-enriched phospholipid ameliorates insulin resistance and lipid metabolism in diet-induced-obese mice. Lipids Health Dis 12(1):109
Millet S, De Ceulaer K, Van Paemel M, Raes K, De Smet S, Janssens GPJ (2006) Lipid profile in eggs of Araucana hens compared with Lohmann Selected Leghorn and ISA Brown hens given diets with different fat sources. Br Poult Sci 47(3):294–300
Caston L, Leeson S (1990) Research note: dietary flax and egg composition. Poult Sci 69(9):1617–1620
Elswyk MEVAN, Dawson PL, Sams AR (1985) Dietary menhaden oil influences sensory characteristics headspace volatiles of shell eggs. J Food Sci 60(7):85–89
Gładkowski W, Kiełbowicz G, Chojnacka A, Gil M, Trziszka T, Dobrzański Z, Wawrzeńczyk C (2011) Fatty acid composition of egg yolk phospholipid fractions following feed supplementation of Lohmann Brown hens with humic-fat preparations. Food Chem 126(3):1013–1018
Vieira PM, Vieira AV, Sanders EJ, Steyrer E, Nimpf J, Schneider WJ (1995) Chicken yolk contains bona fide high density lipoprotein particles. J Lipid Res 36(3):601–610
Baucells MD, Crespo N, Barroeta AC, López-Ferrer S, Grashorn MA (2000) Incorporation of different polyunsaturated fatty acids into eggs. Poult Sci 79(1):51–59
Naber EC, Squires MW (1993) Vitamin profiles of eggs as indicators of nutritional status in the laying hen: diet to egg transfer and commercial flock surve. Poult Sci 72(6):1046–1053
Ayerza R, Coates W, Lauria M (2002) Chia seed (Salvia hispanica L.) as an ω-3 fatty acid source for broilers: influence on fatty acid composition, cholesterol and fat content of white and dark meats, growth performance, and sensory characteristics. Poult Sci 81(6):826–837
Sims JS, Qi GH (1995) Designing poultry products using flaxseed. In: Cunnane SC, Thompson LU (eds) Flaxseed in human nutrition. AOCS Press, Champaign, pp 315–333
Brenner RR (1989) Factors influencing fatty acid chain elongation and desaturation. In: Ergroesen M, Crawford AJ (eds) The role of fats in human nutrition, vol 3, no 1. Academic Press, New York, pp 45–79
Sinanoglou VJ, Strati IF, Miniadis-Meimaroglou S (2011) Lipid, fatty acid and carotenoid content of edible egg yolks from avian species: a comparative study. Food Chem 124(3):971–977
Kuksis A (1992) Yolk lipids. Biochim Biophys Acta—Mol Cell Biol Lipids 1124(3):205–222
Acknowledgments
The authors acknowledge financial support from the Canadian Hemp Trade Alliance (CHTA; Winnipeg, MB, Canada); Canadian Agricultural Adaptation Program (CAAP; Ottawa, ON, Canada) and Province of Manitoba Science and Technology International Collaboration Fund (Winnipeg, MB, Canada). Statistical assistance from Drs. G. H. Crow and L. Onischuk (Department of Animal Science, University of Manitoba), technical assistance from N. Gakhar (Department of Animal Science, University of Manitoba), and support with animal care from J. Levandoski and A. Chartier (Poultry Research Unit, University of Manitoba) are highly appreciated.
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Neijat, M., Suh, M., Neufeld, J. et al. Increasing Levels of Dietary Hempseed Products Leads to Differential Responses in the Fatty Acid Profiles of Egg Yolk, Liver and Plasma of Laying Hens. Lipids 51, 615–633 (2016). https://doi.org/10.1007/s11745-016-4146-9
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DOI: https://doi.org/10.1007/s11745-016-4146-9