Consumption of echium oil increases EPA and DPA in blood fractions more efficiently compared to linseed oil in humans

Katrin Kuhnt, Stefanie Weiß, Michael Kiehntopf, Gerhard Jahreis, Katrin Kuhnt, Stefanie Weiß, Michael Kiehntopf, Gerhard Jahreis

Abstract

Background: A plant-based strategy to improve long-chain (LC) omega (n)-3 PUFA supply in humans involves dietary supplementation with oils containing α-linolenic acid (ALA) alone or in combination with stearidonic acid (SDA). The study aimed to compare the effects of echium oil (EO) and linseed oil (LO) on LC n-3 PUFA accumulation in blood and on clinical markers.

Methods: In two double-blind, parallel-arm, randomized controlled studies, all volunteers started with 17 g/d run-in oil (2 weeks). Thereafter, subjects received diets enriched in study 1 with EO (5 g ALA + 2 g SDA; n = 59) or in study 2 with LO (5 g ALA; n = 9) daily for 8 weeks. The smaller control groups received fish oil (FO; n = 19) or olive oil (OO; n = 18). Participants were instructed to restrict their dietary n-3 PUFA intake throughout the studies (e.g., no fish). To investigate the influence of age and BMI on the conversion of ALA and SDA as well as clinical markers, the subjects recruited for EO and LO treatment were divided into three subgroups (two age groups 20-35 y; 49-69 y with BMI 18-25 kg/m(2) and one group with older, overweight subjects (age 49-69 y; BMI >25 kg/m(2)).

Results: In plasma, red blood cells (RBC), and peripheral blood mononuclear cells (PBMC), EPA and docosapentaenoic acid (DPA) were ~25 % higher following EO compared to LO. Comparing all treatments, the effectiveness of increasing EPA and DPA in plasma, RBC, and PBMC was on average 100:25:10:0 and 100:50:25:0 for FO:EO:LO:OO, respectively. EO led to a lower arachidonic acid/EPA-ratio compared to LO in plasma, RBC, and PBMC. Following EO, final DHA was not greater compared to LO. Higher BMI correlated negatively with increases in plasma EPA and DPA after EO supplementation, but not after LO supplementation. Decreasing effect on plasma LDL-C and serum insulin was greater with EO than with LO.

Conclusions: Daily intake of SDA-containing EO is a better supplement than LO for increasing EPA and DPA in blood. However, neither EO nor LO maintained blood DHA status in the absence of fish/seafood consumption.

Trial registration: ClinicalTrials.gov Reg No. NCT01856179; ClinicalTrials.gov Reg No. NCT01317290.

Figures

Fig. 1
Fig. 1
Flow diagram of subjects through study 1 and study 2. Subjects from study 1 who agreed to a repeat participation were implemented in study 2; former EO subjects were supplemented with LO in study 2; former FO subjects were supplemented with OO in study 2. EO, echium oil; FO, fish oil; LO, linseed oil mixture; OO, olive oil. Subgroup I, age 20–35 years and BMI 18–25 kg/m2; subgroup II, age 49–69 years and BMI 18–25 kg/m2; subgroup III, age 49–69 years and BMI >25 kg/m2
Fig. 2
Fig. 2
Final AA/EPA ratio in plasma, RBC, and PBMC in subjects following 8 weeks of fish oil, echium oil, linseed oil mixture, or olive oil. Values are means ± SEM. P values were analyzed using the generalized linear mixed model ANCOVA with sex, age, BMI, and baseline value as covariates. abcWithin one blood fraction, means with different superscript letters are significantly different between treatment groups (P ≤ 0.05). ***Means are significantly different between EO and LO treatment (P < 0.001; ‡P 0.05 < 0.10). AA, arachidonic acid; EO, echium oil; FO, fish oil; LO, linseed oil; OO, olive oil

References

    1. Mozaffarian D, Wu JH. Omega-3 fatty acids and CVD: effects on risk factors, molecular pathways, and clinical events. J Am Coll Cardiol. 2011;58:2047–67. doi: 10.1016/j.jacc.2011.06.063.
    1. Harris WS. The omega-3 index: from biomarker to risk marker to risk factor. Curr Atheroscler Rep. 2009;11:411–7. doi: 10.1007/s11883-009-0062-2.
    1. Kris-Etherton PM, Harris WS, Appel LJ; American Heart Association. Nutrition Committee. Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation 2002;106:2747–57.
    1. Barceló-Coblijn G, Murphy EJ. 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. 2009;48:355–74. doi: 10.1016/j.plipres.2009.07.002.
    1. Brenna JT, Salem N, Jr, Sinclair AJ, Cunnane SC, International Society for the Study of Fatty Acids and Lipids, ISSFAL alpha-Linolenic acid supplementation and conversion to n-3 long-chain polyunsaturated fatty acids in humans. Prostaglandins Leukot Essent Fatty Acids. 2009;80:85–91. doi: 10.1016/j.plefa.2009.01.004.
    1. Burdge GC, Calder PC. Conversion of alpha-linolenic acid to longer-chain polyunsaturated fatty acids in human adults. Reprod Nutr Dev. 2005;45:581–97. doi: 10.1051/rnd:2005047.
    1. Blasbalg TL, Hibbeln JR, Ramsden CE, Majchrzak SF, Rawlings RR. Changes in consumption of omega-3 and omega-6 fatty acids in the United States during the 20th century. Am J Clin Nutr. 2011;93:950–62. doi: 10.3945/ajcn.110.006643.
    1. Simopoulos AP. The importance of the omega-6/omega-3 fatty acid ratio in cardiovascular disease and other chronic diseases. Exp Biol Med. 2008;233:674–88. doi: 10.3181/0711-MR-311.
    1. Venegas-Calerón M, Sayanova O, Napier JA. An alternative to fish oils: metabolic engineering of oil-seed crops to produce omega-3 long chain polyunsaturated fatty acids. Prog Lipid Res. 2010;49:108–19. doi: 10.1016/j.plipres.2009.10.001.
    1. Guil-Guerrero JL. Stearidonic acid (18:4n-3): Metabolism, nutritional importance, medical uses and natural sources. Eur J Lipid Sci Technol. 2007;109:1226–36. doi: 10.1002/ejlt.200700207.
    1. Kuhnt K, Degen C, Jaudszus A, Jahreis G. Searching for health beneficial n-3 and n-6 fatty acids in plant seeds. Eur J Lipid Sci Technol. 2012;114:153–60. doi: 10.1002/ejlt.201100008.
    1. James MJ, Ursin VM, Cleland LG. Metabolism of stearidonic acid in human subjects: comparison with the metabolism of other n-3 fatty acids. Am J Clin Nutr. 2003;77:1140–5.
    1. Ruiz-Lopez N, Haslam RP, Venegas-Caleron M, Larson TR, Graham IA, Napier JA, Sayanova O. The synthesis and accumulation of stearidonic acid in transgenic plants: a novel source of ‘heart-healthy’ omega-3 fatty acids. Plant Biotechnol J. 2009;7:704–16. doi: 10.1111/j.1467-7652.2009.00436.x.
    1. Harris WS. Stearidonic acid-enhanced soybean oil: a plant-based source of (n-3) fatty acids for foods. J Nutr. 2012;142:600S–4. doi: 10.3945/jn.111.146613.
    1. Harris WS, Lemke SL, Hansen SN, Goldstein DA, DiRienzo MA, Su H, Nemeth MA, Taylor ML, Ahmed G, George C. Stearidonic acid-enriched soybean oil increased the omega-3 index, an emerging cardiovascular risk marker. Lipids. 2008;43:805–11. doi: 10.1007/s11745-008-3215-0.
    1. Lemke SL, Vicini JL, Su H, Goldstein DA, Nemeth MA, Krul ES, Harris WS. Dietary intake of stearidonic acid-enriched soybean oil increases the omega-3 index: randomized, double-blind clinical study of efficacy and safety. Am J Clin Nutr. 2010;92:766–75. doi: 10.3945/ajcn.2009.29072.
    1. Krul ES, Lemke SL, Mukherjea R, Taylor ML, Goldstein DA, Su H, Liu P, Lawless A, Harris WS, Maki KC. Effects of duration of treatment and dosage of eicosapentaenoic acid and stearidonic acid on red blood cell eicosapentaenoic acid content. Prostaglandins Leukot Essent Fatty Acids. 2012;86:51–9. doi: 10.1016/j.plefa.2011.10.005.
    1. Surette ME, Edens M, Chilton FH, Tramposch KM. Dietary echium oil increases plasma and neutrophil long-chain (n-3) fatty acids and lowers serum triacylglycerols in hypertriglyceridemic humans. J Nutr. 2004;134:1406–11.
    1. Zhang P, Boudyguina E, Wilson MD, Gebre AK, Parks JS. Echium oil reduces plasma lipids and hepatic lipogenic gene expression in apoB100-only LDL receptor knockout mice. J Nutr Biochem. 2008;19:655–63. doi: 10.1016/j.jnutbio.2007.08.005.
    1. Kuhnt K, Fuhrmann C, Köhler M, Kiehntopf M, Jahreis G. Dietary echium oil increases long-chain n-3 PUFA including docosapentaenoic acid in blood fractions and alters biochemical markers for CVD independent of age, sex, and metabolic syndrome. J Nutr. 2014;144:447–60. doi: 10.3945/jn.113.180802.
    1. Grindel A, Staps F, Kuhnt K. Cheek cell fatty acids reflect n-3 PUFA in blood fractions during linseed oil supplementation: a controlled human intervention study. Lipids Health Dis. 2013;12:173. doi: 10.1186/1476-511X-12-173.
    1. Kuhnt K, Kraft J, Moeckel P, Jahreis G. Trans-11-18:1 is effectively Delta9-desaturated compared with trans-12-18:1 in humans. Br J Nutr. 2006;95:752–61. doi: 10.1079/BJN20051680.
    1. Dubois V, Breton S, Linder M, Fanni J, Parmentier M. Fatty acid profiles of 80 vegetable oils with regard to their nutritional potential. Eur J Lipid Sci Technol. 2007;109:710–32. doi: 10.1002/ejlt.200700040.
    1. Kitessa SM, Young P, Nattrass G, Gardner G, Pearce K, Pethick DW. When balanced for precursor fatty acid supply echium oil is not superior to linseed oil in enriching lamb tissues with long-chain n-3 PUFA. Br J Nutr. 2012;108:71–9. doi: 10.1017/S0007114511005411.
    1. Poudyal H, Panchal SK, Diwan V, Brown L. Omega-3 fatty acids and metabolic syndrome: effects and emerging mechanisms of action. Prog Lipid Res. 2011;50:372–87. doi: 10.1016/j.plipres.2011.06.003.
    1. Arab L. Biomarkers of fat and fatty acid intake. J Nutr. 2003;133(Suppl 3):925S–32.
    1. Finnegan YE, Minihane AM, Leigh-Firbank EC, Kew S, Meijer GW, Muggli R, Calder PC, Williams CM. Plant- and marine-derived n-3 polyunsaturated fatty acids have differential effects on fasting and postprandial blood lipid concentrations and on the susceptibility of LDL to oxidative modification in moderately hyperlipidemic subjects. Am J Clin Nutr. 2003;77:783–95.
    1. Dewell A, Marvasti FF, Harris WS, Tsao P, Gardner CD. Low- and high-dose plant and marine (n-3) fatty acids do not affect plasma inflammatory markers in adults with metabolic syndrome. J Nutr. 2011;141:2166–71. doi: 10.3945/jn.111.142240.
    1. Patenaude A, Rodriguez-Leyva D, Edel AL, Dibrov E, Dupasquier CM, Austria JA, Richard MN, Chahine MN, Malcolmson LJ, Pierce GN. Bioavailability of alpha-linolenic acid from flaxseed diets as a function of the age of the subject. Eur J Clin Nutr. 2009;63:1123–9. doi: 10.1038/ejcn.2009.41.
    1. Portolesi R, Powell BC, Gibson RA. Competition between 24:5n-3 and ALA for Delta 6 desaturase may limit the accumulation of DHA in HepG2 cell membranes. J Lipid Res. 2007;48:1592–8. doi: 10.1194/jlr.M700081-JLR200.
    1. Vermunt SHF, Mensink RP, Simonis MMG, Hornstra G. Effects of dietary alpha-linolenic acid on the conversion and oxidation of C-13-alpha-linolenic acid. Lipids. 2000;35:137–42. doi: 10.1007/BF02664762.
    1. Goyens P, Spilker M, Zock P, Katan M, Mensink R. Conversion of alpha-linolenic acid in humans is influenced by the absolute amounts of alpha-linolenic acid and linoleic acid in the diet and not by their ratio. Am J Clin Nutr. 2006;84:44–53.
    1. Emken EA, Adlof RO, Gulley RM. Dietary linoleic acid influences desaturation and acylation of deuterium-labeled linoleic and linolenic acids in young adult males. Biochim Biophys Acta. 1994;1213:277–88. doi: 10.1016/0005-2760(94)00054-9.
    1. Gillingham LG, Harding SV, Rideout TC, Yurkova N, Cunnane SC, Eck PK, Jones PJ. Dietary oils and FADS1-FADS2 genetic variants modulate [13C]α-linolenic acid metabolism and plasma fatty acid composition. Am J Clin Nutr. 2013;97:195–207. doi: 10.3945/ajcn.112.043117.
    1. Stanley JC, Elsom RL, Calder PC, Griffin BA, Harris WS, Jebb SA, Lovegrove JA, Moore CS, Riemersma RA, Sanders TA. UK Food Standards Agency Workshop Report: the effects of the dietary n-6:n-3 fatty acid ratio on cardiovascular health. Br J Nutr. 2007;98:1305–10. doi: 10.1017/S000711450784284X.
    1. Surette ME. Dietary omega-3 PUFA and health: stearidonic acid-containing seed oils as effective and sustainable alternatives to traditional marine oils. Mol Nutr Food Res. 2013;57:748–59. doi: 10.1002/mnfr.201200706.
    1. Childs CE, Romeu-Nadal M, Burdge GC, Calder PC. Gender differences in the n-3 fatty acid content of tissues. Proc Nutr Soc. 2008;67:19–27. doi: 10.1017/S0029665108005983.
    1. Burdge G. Alpha-linolenic acid metabolism in men and women: nutritional and biological implications. Curr Opin Clin Nutr Metab Care. 2004;7:137–44. doi: 10.1097/00075197-200403000-00006.
    1. Sands SA, Reid KJ, Windsor SL, Harris WS. The impact of age, body mass index, and fish intake on the EPA and DHA content of human erythrocytes. Lipids. 2005;40:343–7. doi: 10.1007/s11745-006-1392-2.
    1. Casey JM, Banz WJ, Krul ES, Butteiger DN, Goldstein DA, Davis JE. Effect of stearidonic acid-enriched soybean oil on fatty acid profile and metabolic parameters in lean and obese Zucker rats. Lipids Health Dis. 2013;12:147. doi: 10.1186/1476-511X-12-147.
    1. Barceló-Coblijn G, Murphy EJ, Othman R, Moghadasian MH, Kashour T, Friel JK. Flaxseed oil and fish-oil capsule consumption alters human red blood cell n-3 fatty acid composition: a multiple-dosing trial comparing 2 sources of n-3 fatty acid. Am J Clin Nutr. 2008;88:801–9.
    1. Kaul N, Kreml R, Austria JA, Richard MN, Edel AL, Dibrov E, Hirono S, Zettler ME, Pierce GN. A comparison of fish oil, flaxseed oil and hempseed oil supplementation on selected parameters of cardiovascular health in healthy volunteers. J Am Coll Nutr. 2008;27:51–8. doi: 10.1080/07315724.2008.10719674.
    1. Sioen I, Hacquebard M, Hick G, Maindiaux V, Larondelle Y, Carpentier YA, De Henauw S. Effect of ALA-enriched food supply on cardiovascular risk factors in males. Lipids. 2009;44:603–11. doi: 10.1007/s11745-009-3307-5.
    1. Bloedon LT, Balikai S, Chittams J, Cunnane SC, Berlin JA, Rader DJ, Szapary PO. Flaxseed and cardiovascular risk factors: results from a double-blind, randomized, controlled clinical trial. J Am Coll Nutr. 2008;27:65–74. doi: 10.1080/07315724.2008.10719676.
    1. Santana O, Reina M, Braulio MF, Sanz J, Gonzalez-Coloma A. Antifeedant activity of fatty acid esters and phytosterols from Echium wildpretii. Chem Biodivers. 2012;9:567–76. doi: 10.1002/cbdv.201100083.
    1. Banz WJ, Davis JE, Clough RW, Cheatwood JL. Stearidonic acid: is there a role in the prevention and management of type 2 diabetes mellitus? J Nutr. 2012;142:635S–40. doi: 10.3945/jn.111.146829.
    1. Wang C, Harris WS, Chung M, Lichtenstein AH, Balk EM, Kupelnick B, Jordan HS, Lau J. n-3 Fatty acids from fish or fish-oil supplements, but not alpha-linolenic acid, benefit cardiovascular disease outcomes in primary- and secondary-prevention studies: a systematic review. Am J Clin Nutr. 2006;84:5–17.

Source: PubMed

Подписаться