Changes in fatty acid levels after consumption of a novel docosahexaenoic supplement from algae: a crossover randomized controlled trial in omnivorous, lacto-ovo vegetarians and vegans

Elena García-Maldonado, Alexandra Alcorta, Belén Zapatera, M Pilar Vaquero, Elena García-Maldonado, Alexandra Alcorta, Belén Zapatera, M Pilar Vaquero

Abstract

Purpose: To determine serum fatty acids of lacto-ovo vegetarian (LOV), vegan (VEG) and omnivorous (OMN) adults, and to analyse the effects of consuming a docosahexaenoic acid (DHA) supplement of vegetable origin on fatty acid profile.

Methods: A randomized, double-blind, placebo-controlled crossover design was conducted in healthy adults. Volunteers (n = 116) were randomly assigned to a DHA-supplement (dose 250 mg/day), made from the microalgae Schizochytrium sp., or a placebo during 5-week periods separated by a 5-week washout interim period. Compliance and dietary intake were estimated and serum fatty acids were determined by gas chromatography. Results were analysed by mixed linear models.

Results: Percentage of linoleic acid (C18:2n6) in serum was the highest among the fatty acids in the three diet groups, followed by oleic (C18:1n9) and palmitic (C16:0) acids. Linoleic (C18:2n6) and alpha-linolenic (C18:3n3) acids were higher in VEG compared to OMN (p < 0.001), while in LOV, their levels were intermediate between the other groups. Women presented higher DHA (C22:6n3) than men (p < 0.001). The DHA-supplement increased serum DHA compared to placebo in the three diet groups (p < 0.001), and a higher increase was observed in VEG followed by LOV (p < 0.001). The ratio serum n-6/n-3 improved by the supplementation but remained higher in LOV and VEG than in OMN. In contrast, the DHA-supplement decreased docosapentaenoic (C22:5n3) and docosatetraenoic (C22:4n6) acids in all diet groups (p < 0.001) and increased the eicosapentaenoic to alpha-linolenic fatty acids ratio (p = 0.016).

Conclusion: The DHA-supplement at dose of 250 mg/day was effective in increasing serum DHA either in omnivorous, lacto-ovo vegetarian and vegan adults.

Clinical trial registration: Registered at Clinicaltrials.gov ( www.

Clinicaltrials: gov ), NCT04278482.

Keywords: Docosahexaenoic acid; Fatty acids; Omega-3; Omega-6; Supplementation; Vegan; Vegetarian.

Conflict of interest statement

The authors declare that they have no conflicts of interest.

© 2022. The Author(s).

Figures

Fig. 1
Fig. 1
Consolidated Standards for Reporting Trials (CONSORT) flow diagram
Fig. 2
Fig. 2
Change in serum DHA after intake the DHA-supplement or placebo, according to diet group and gender. OMN omnivorous, LOV lacto-ovo vegetarian, VEG vegan. All three diet groups were significantly different after DHA-supplement (p < 0.001) and there were no significant differences between diet groups after placebo. The differences between men and women were not significant (ANOVA)
Fig.3
Fig.3
Biosynthesis of long chain polyunsaturated fatty acids in humans and changes due to vegetarian diets and DHA supplementation of the present randomized controlled trial. Fatty acids analyzed in this study are in bold. Δ6: desaturase Δ6; Δ5: desaturase Δ5; Δ: desaturase Δ9; Elon: elongase. Differences due to diet type: open arrows indicate significantly increased or decreased in lacto-ovo vegetarians and/or vegans compared to omnivorous. Changes due to the DHA supplementation: dark arrows indicate significant increase or decrease after consumption of the DHA-supplement in the three diet groups

References

    1. Dinu M, Abbate R, Gensini GF, et al. Vegetarian, vegan diets and multiple health outcomes: a systematic review with meta-analysis of observational studies. Crit Rev Food Sci Nutr. 2017;57:3640–3649. doi: 10.1080/10408398.2016.1138447.
    1. Craddock JC, Neale EP, Probst YC, Peoples GE. Algal supplementation of vegetarian eating patterns improves plasma and serum docosahexaenoic acid concentrations and omega-3 indices: a systematic literature review. J Hum Nutr Diet. 2017;30:693–699. doi: 10.1111/jhn.12474.
    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;48:355–374. doi: 10.1016/j.plipres.2009.07.002.
    1. Brenna JT. Efficiency of conversion of α-linolenic acid to long chain n-3 fatty acids in man. Curr Opin Clin Nutr Metab Care. 2002;5:127–132. doi: 10.1097/00075197-200203000-00002.
    1. Burdge GC, Wootton SA. Conversion of α-linolenic acid to eicosapentaenoic, docosapentaenoic and docosahexaenoic acids in young women. Br J Nutr. 2002;88:411–420. doi: 10.1079/BJN2002689.
    1. Rosell MS, Lloyd-Wright Z, Appleby PN, et al. Long-chain n–3 polyunsaturated fatty acids in plasma in British meat-eating, vegetarian, and vegan men. Am J Clin Nutr. 2005;82:327–334. doi: 10.1093/ajcn/82.2.327.
    1. Sanders TAB. DHA status of vegetarians. Prostaglandins Leukot Essent Fatty Acids. 2009;81(2–3):137–141. doi: 10.1016/j.plefa.2009.05.013.
    1. Salvador AM, García-Maldonado E, Gallego-Narbón A, et al. Fatty acid profile and cardiometabolic markers in relation with diet type and omega-3 supplementation in Spanish vegetarians. Nutrients. 2019;11:1659. doi: 10.3390/nu11071659.
    1. Matos ÂP. The impact of microalgae in food science and technology. J Am Oil Chem Soc. 2017;94:1333–1350. doi: 10.1007/s11746-017-3050-7.
    1. Commission Commission implementing decision of 14 July 2014 on authorising the placing on the market of oil from the micro-algae Schizochytrium sp. as a novel food ingredient under Regulation (EC) No 258/97 of the European Parliament and of the Council and repealing Decisions 2003/427/EC and 2009/778/EC. Official Journal of the European Union L 209/56
    1. EFSA Panel on Dietetic Products Nutrition and allergies (NDA) Scientific opinion related to the tolerable upper intake level of eicosapentaenoic acid (EPA) docosahexaenoic acid (DHA) and docosapentaenoic acid (DPA) EFSA J. 2012;10(7):48. doi: 10.2903/j.efsa.2012.2815.
    1. EFSA Panel on Dietetic Products Nutrition and Allergies (NDA) Scientific opinion the substantiation of a health claim related to docosahexaenoic acid (DHA) and maintenance of normal (fasting) blood concentrations of triglycerides (ID 533, 691, 3150), protection of blood lipids from oxidative damage (ID 630), contribution to the maintenance or achievement of a normal body weight (ID 629), brain, eye and nerve development (ID 627, 689, 704, 742, 3148, 3151), maintenance of normal brain function (ID 565, 626, 631, 689, 690, 704, 742, 3148, 3151), maintenance of normal vision (ID 627, 632, 743, 3149) and maintenance of normal spermatozoa motility (ID 628) pursuant to Article 13(3) of Regulation (EC) No 1924/2006. EFSA J. 2010;8(10):27. doi: 10.2903/j.efsa.2010.1734.
    1. McLennan PL. Cardiac physiology and clinical efficacy of dietary fish oil clarified through cellular mechanisms of omega-3 polyunsaturated fatty acids. Eur J Appl Physiol. 2014;114:1333–1356. doi: 10.1007/s00421-014-2876-z.
    1. Conquer JA, Holub BJ. Dietary docosahexaenoic acid as a source of eicosapentaenoic acid in vegetarians and omnivores. Lipids. 1997;32:341–345. doi: 10.1007/s11745-997-0043-y.
    1. Conquer JA, Holub BJ. Supplementation with an algae source of docosahexaenoic acid increases (n-3) fatty acid status and alters selected risk factors for heart disease in vegetarian subjects. J Nutr. 1996;126:3032–3039. doi: 10.1093/jn/126.12.3032.
    1. Wu WH, Lu SC, Wang TF, et al. Effects of docosahexaenoic acid supplementation on blood lipids, estrogen metabolism, and in vivo oxidative stress in postmenopausal vegetarian women. Eur J Clin Nutr. 2006;60:386–392. doi: 10.1038/sj.ejcn.1602328.
    1. Stark KD, Holub BJ. Differential eicosapentaenoic acid elevations and altered cardiovascular disease risk factor responses after supplementation with docosahexaenoic acid in postmenopausal women receiving and not receiving hormone replacement therapy. Am J Clin Nutr. 2004;79:765–773. doi: 10.1093/ajcn/79.5.765.
    1. Arterburn LM, Oken HA, Hoffman JP, et al. Bioequivalence of docosahexaenoic acid from different algal oils in capsules and in a DHA-fortified food. Lipids. 2007;42:1011. doi: 10.1007/s11745-007-3098-5.
    1. Sarter B, Kelsey KS, Schwartz TA, Harris WS. Blood docosahexaenoic acid and eicosapentaenoic acid in vegans: associations with age and gender and effects of an algal-derived omega-3 fatty acid supplement. Clin Nutr. 2015;34:212–218. doi: 10.1016/j.clnu.2014.03.003.
    1. Bartrina J, Arija V, Maiz E, et al. Guías alimentarias para la población española (SENC, diciembre 2016); la nueva pirámide de la alimentación saludable. Nutr Hosp. 2017;33(8):1–48.
    1. Stonehouse W, Klingner B, Tso R, et al. Bioequivalence of long-chain omega-3 polyunsaturated fatty acids from foods enriched with a novel vegetable-based omega-3 delivery system compared to gel capsules: a randomized controlled cross-over acute trial. Eur J Nutr. 2022;61(4):2129–2141. doi: 10.1007/s00394-021-02795-7.
    1. Lane K, Derbyshire E, Li W, Brennan C. Bioavailability and potential uses of vegetarian sources of omega-3 fatty acids: a review of the literature. Crit Rev Food Sci Nutr. 2014;54:572–579. doi: 10.1080/10408398.2011.596292.
    1. Lee MRF, Tweed JKS, Kim EJ, Scollan ND. Beef, chicken and lamb fatty acid analysis—a simplified direct bimethylation procedure using freeze-dried material. Meat Sci. 2012;92:863–866. doi: 10.1016/j.meatsci.2012.06.013.
    1. Elorinne A-L, Alfthan G, Erlund I, et al. Food and nutrient intake and nutritional status of Finnish vegans and non-vegetarians. PLoS ONE. 2016;11:e0148235–e0148235. doi: 10.1371/journal.pone.0148235.
    1. Zazpe I, Sanchez-Tainta A, Estruch R, et al. A large randomized individual and group intervention conducted by registered dietitians increased adherence to Mediterranean-type diets: the PREDIMED study. J Am Diet Assoc. 2008;108:1134–1144. doi: 10.1016/j.jada.2008.04.011.
    1. Ruiz E, Ávila JM, Valero T, et al. Energy intake, profile, and dietary sources in the Spanish population: findings of the ANIBES study. Nutrients. 2015;7(6):4739–4762. doi: 10.3390/nu7064739.
    1. EFSA Panel on Dietetic Products Nutrition and Allergies (NDA) Scientific opinion on dietary reference values for fats, including saturated fatty acids, polyunsaturated fatty acids, monounsaturated fatty acids, trans fatty acids, and cholesterol. EFSA J. 2010;8(3):107. doi: 10.2903/j.efsa.2010.1461.
    1. Simopoulos AP. The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed Pharmacother. 2002;56:365–379. doi: 10.1016/S0753-3322(02)00253-6.
    1. Greupner T, Kutzner L, Pagenkopf S, et al. Effects of a low and a high dietary LA/ALA ratio on long-chain PUFA concentrations in red blood cells. Food Funct. 2018;9:4742–4754. doi: 10.1039/C8FO00735G.
    1. Craddock J, Probst Y, Neale E, Peoples G. A cross-sectional comparison of the whole blood fatty acid profile and omega-3 index of male vegan and omnivorous endurance athletes. J Am Coll Nutr. 2022;41:333–341.
    1. Brenna JT, Plourde M, Stark KD, et al. Best practices for the design, laboratory analysis, and reporting of trials involving fatty acids. Am J Clin Nutr. 2018;108:211–227. doi: 10.1093/ajcn/nqy089.
    1. Alessandri J-M, Extier A, Al-Gubory KH, et al. Influence of gender on DHA synthesis: the response of rat liver to low dietary α-linolenic acid evidences higher ω3 ∆4-desaturation index in females. Eur J Nutr. 2012;51:199–209. doi: 10.1007/s00394-011-0208-1.
    1. Dyall SC. Long-chain omega-3 fatty acids and the brain: a review of the independent and shared effects of EPA. DPA DHA Front Aging Neurosci. 2015;21(7):52.
    1. Drouin G, Rioux V, Legrand P. The n-3 docosapentaenoic acid (DPA): a new player in the n-3 long chain polyunsaturated fatty acid family. Fat Acids Lipopolysaccharides Health Dis. 2019;159:36–48.
    1. Plourde M, Cunnane SC. Extremely limited synthesis of long chain polyunsaturates in adults: implications for their dietary essentiality and use as supplements. Appl Physiol Nutr Metab. 2007;32:619–634. doi: 10.1139/H07-034.
    1. Slee EL, McLennan PL, Owen AJ, Theiss ML. Low dietary fish-oil threshold for myocardial membrane n-3 PUFA enrichment independent of n-6 PUFA intake in rats. J Lipid Res. 2010;51:1841–1848. doi: 10.1194/jlr.M004069.
    1. Stark KD, Van Elswyk ME, Higgins MR, et al. Global survey of the omega-3 fatty acids, docosahexaenoic acid and eicosapentaenoic acid in the blood stream of healthy adults. Prog Lipid Res. 2016;63:132–152. doi: 10.1016/j.plipres.2016.05.001.
    1. Stark KD, Aristizabal Henao JJ, Metherel AH, Pilote L. Translating plasma and whole blood fatty acid compositional data into the sum of eicosapentaenoic and docosahexaenoic acid in erythrocytes. Prostaglandins Leukot Essent Fatty Acids. 2016;104:1–10. doi: 10.1016/j.plefa.2015.11.002.
    1. Kuhnt K, Fuhrmann C, Köhler M, et al. Dietary echium oil increases long-chain n-3 PUFAs, including docosapentaenoic acid, in blood fractions and alters biochemical markers for cardiovascular disease independent of age, sex, and metabolic syndrome. J Nutr. 2014;144(4):447–460. doi: 10.3945/jn.113.180802.
    1. Metherel AH, Irfan M, Klingel SL, et al. Compound-specific isotope analysis reveals no retroconversion of DHA to EPA but substantial conversion of EPA to DHA following supplementation: a randomized control trial. Am J Clin Nutr. 2019;110:823–831. doi: 10.1093/ajcn/nqz097.
    1. Brenna JT. DHA retroconversion revisited: dietary DHA spares endogenous EPA. Am J Clin Nutr. 2019;110:789–790. doi: 10.1093/ajcn/nqz125.
    1. Geppert J, Kraft V, Demmelmair H, Koletzko B. Microalgal docosahexaenoic acid decreases plasma triacylglycerol in normolipidaemic vegetarians: a randomised trial. Br J Nutr. 2006;95:779–786. doi: 10.1079/BJN20051720.
    1. Sanders TAB, Gleason K, Griffin B, Miller GJ. Influence of an algal triacylglycerol containing docosahexaenoic acid (22:6n–3) and docosapentaenoic acid (22:5n–6) on cardiovascular risk factors in healthy men and women. Br J Nutr. 2006;95:525–531. doi: 10.1079/BJN20051658.
    1. Alcorta A, Porta A, Tárrega A, Alvarez MD, Vaquero MP. Foods for plant-based diets: challenges and innovations. Foods. 2021;10(2):293. doi: 10.3390/foods10020293.

Source: PubMed

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