Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Change in the fatty acid pattern of erythrocyte membrane phospholipids after oral supplementation of specific fatty acids in patients with gastrointestinal diseases

European Journal of Clinical Nutrition volume 64, pages 410–418 (2010)Cite this article

Subjects

Abstract

Background/Objectives:

The fatty acid pattern of membrane phospholipids is suggested to affect membrane fluidity and epithelial barrier function as a result of membrane fatty acid unsaturation. The incorporation of n-3 polyunsaturated fatty acids (PUFAs) into membrane phospholipids may diminish inflammatory potential in patients with gastrointestinal diseases. The aim of this study was to improve the fatty acid profile of erythrocyte membrane phospholipids after oral supplementation of specific fatty acids in patients with maldigestion and/or malabsorption.

Subjects/Methods:

We conducted a randomized, double-blind, controlled trial. A total of 48 patients with gastrointestinal diseases received either fat-soluble vitamins A,D,E,K (ADEK) or ADEK plus fatty acids α-linolenic acid (ALA), docosahexaenoic acid (DHA) and medium-chain triglycerides (FA-ADEK) for 12 weeks. The fatty acid profile of erythrocyte membrane phospholipids, dietary intake, plasma antioxidant vitamins and serum γ-glutamyl transferase (GGT) were evaluated at baseline, 8 and 12 weeks after supplementation.

Results:

Supplementation with FA-ADEK increased ALA, DHA and eicosapentaenoic acid (EPA) concentrations of erythrocyte membrane phospholipids by 0.040, 1.419 and 0.159%, respectively, compared with ADEK supplementation (−0.007, 0.151 and 0.002%, respectively) after 12 weeks (all P⩽0.001). Serum GGT activity decreased in patients receiving FA-ADEK compared with those receiving ADEK with a significant difference after 8 weeks.

Conclusions:

The significant change in erythrocyte membrane fatty acid pattern demonstrates the incorporation of orally administered n-3 PUFA in patients with maldigestion and malabsorption. The increase in ALA and DHA, as well as the conversion of ALA to EPA is attributed to the supplementation of sufficient amounts of ALA and DHA, respectively. Serum GGT activity decreased in response to decreased oxidative stress.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2

Similar content being viewed by others

References

  • André P, Balkau B, Born C, Charles MA, Eschwège E, D.E.S.I.R. study group (2006). Three-year increase of gamma-glutamyltransferase level and development of type 2 diabetes in middle-aged men and women: the D.E.S.I.R. cohort. Diabetologia 49, 2599–2603.

    Article  PubMed  PubMed Central  Google Scholar 

  • Barceló-Coblijn G, Murphy EJ, Othman R, Moghadasian MH, Kashour T, Friel JK (2008). 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 88, 801–809.

    Article  PubMed  Google Scholar 

  • Belluzzi A, Brignola C, Campieri M, Pera A, Boschi S, Miglioli M (1996). Effect of an enteric-coated fish-oil preparation on relapses in Crohn's disease. N Engl J Med 334, 1557–1560.

    Article  CAS  PubMed  Google Scholar 

  • Biesalski HK, Böhles H, Esterbauer H, Fürst P, Gey F, Hundsdörfer G et al. (1997). Antioxidant vitamins in prevention. Clin Nutr 16, 151–155.

    Article  CAS  PubMed  Google Scholar 

  • Calder PC (2008). Polyunsaturated fatty acids, inflammatory processes and inflammatory bowel diseases. Mol Nutr Food Res 52, 885–897.

    Article  CAS  PubMed  Google Scholar 

  • Cao J, Schwichtenberg KA, Hanson NQ, Tsai MY (2006). Incorporation and clearance of omega-3 fatty acids in erythrocyte membranes and plasma phospholipids. Clin Chem 52, 2265–2272.

    Article  CAS  PubMed  Google Scholar 

  • Carroccio A, Verghi F, Santini B, Lucidi V, Iacono G, Cavataio F et al. (2001). Diagnostic accuracy of fecal elastase 1 assay in patients with pancreatic maldigestion or intestinal malabsorption. Dig Dis Sci 46, 1335–1342.

    Article  CAS  PubMed  Google Scholar 

  • Christophe A, Matthijs F (1967). New method for the determination of the fatty acid pattern of serum lipid classes. Clin Chim Acta 16, 39–43.

    Article  CAS  PubMed  Google Scholar 

  • Das UN (2006). Essential fatty acids: biochemistry, physiology and pathology. Biotechnol J 1, 420–439.

    Article  CAS  PubMed  Google Scholar 

  • DeMeo MT, Mutlu EA, Keshavarzian A, Tobin MC (2002). Intestinal permeation and gastrointestinal disease. J Clin Gastroenterol 34, 385–396.

    Article  PubMed  Google Scholar 

  • De Vizia B, Raia V, Spano C, Pavlidis C, Coruzzo A, Alessio M (2003). Effect of an 8-month treatment with ω-3 fatty acids (eicosapentaenoic and docosahexaenoic) in patients with cystic fibrosis. J Parenter Enteral Nutr 27, 52–57.

    Article  CAS  Google Scholar 

  • D’Odorico A, Bortolan S, Cardin R, D’Inca R, Martines D, Ferronato A et al. (2001). Reduced plasma antioxidant concentrations and increased oxidative DNA damage in inflammatory bowel disease. Scand J Gastroenterol 36, 1289–1294.

    Article  PubMed  Google Scholar 

  • Ehrhardt J (2002). Labormethoden und Normalwerte für fett- und wasserlösliche Vitamine (Laboratory methods and normal values for fat- and water-soluble vitamins). Vitamine, Spurenelemente und Mineralstoffe. Prävention und Therapie mit Mikronährstoffen (Vitamins, trace elements and minerals. Prevention and therapy with micronutrients), In: (eds). KH Biesalski, J Köhrle, K Schümann, Georg Thieme Verlag: Stuttgart, 676–682.

    Google Scholar 

  • Emdin M, Pompella A, Paolicchi A (2005). Gamma-glutamyltransferase, atherosclerosis, and cardiovascular disease. Triggering oxidative stress within the plaque. Circulation 112, 2078–2080.

    Article  PubMed  Google Scholar 

  • Folch J, Lees M, Stanley GHS (1957). A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226, 497–509.

    CAS  PubMed  Google Scholar 

  • Guebre-Egziabher F, Rabasa-Lhoret R, Bonnet F, Bastard JP, Desage M, Skilton MR et al. (2008). Nutritional intervention to reduce the n-6/n-3 fatty acid ratio increases adiponectin concentration and fatty acid oxidation in healthy subjects. Eur J Clin Nutr 62, 1287–1293.

    Article  CAS  PubMed  Google Scholar 

  • Harats D, Dabach Y, Hollander G, Ben-Naim M, Schwartz R, Berry EM et al. (1991). Fish oil ingestion in smokers and nonsmokers enhances peroxidation of plasma lipoproteins. Atherosclerosis 90, 127–139.

    Article  CAS  PubMed  Google Scholar 

  • Harris WS, Mozaffarian D, Rimm E, Kris-Etherton P, Rudel LL, Appel LJ et al. (2009). Omega-6 fatty acids and risk for cardiovascular disease. A science advisory from the American Heart Association Nutrition Subcommittee of the Council on Nutrition, Physical Activity, and Metabolism; Council on Cardiovascular Nursing; and Council on Epidemiology and Prevention. Circulation 119, 902–907.

    Article  PubMed  Google Scholar 

  • Higdon JV, Liu J, Du SH, Morrow JD, Ames BN, Wander RC (2000). Supplementation of postmenopausal women with fish oil rich in eicosapentaenoic acid and docosahexaenoic acid is not associated with greater in vivo lipid peroxidation compared with oils rich in oleate and linoleate as assessed by plasma malondialdehyde and F2-isoprostanes. Am J Clin Nutr 72, 714–722.

    Article  CAS  PubMed  Google Scholar 

  • Hillier K, Jewell R, Dorrell L, Smith CL (1991). Incorporation of fatty acids from fish oil and olive oil into colonic mucosal lipids and effects upon eicosanoid synthesis in inflammatory bowel disease. Gut 32, 1151–1155.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hull J, Vervaart P, Grimwood K, Phelan P (1997). Pulmonary oxidative stress response in young children with cystic fibrosis. Thorax 52, 557–560.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hussein N, Ah-Sing E, Wilkinson P, Leach C, Griffin BA, Millward DJ (2005). Long-chain conversion of (13C)linoleic acid and α-linolenic acid in response to marked changes in their dietary intake in men. J Lipid Res 46, 269–280.

    Article  CAS  PubMed  Google Scholar 

  • Koutroubakis IE, Malliaraki N, Dimoulios PD, Karmiris K, Castanas E, Kouroumalis EA (2004). Decreased total and corrected antioxidant capacity in patients with inflammatory bowel disease. Dig Dis Sci 49, 1433–1437.

    Article  CAS  PubMed  Google Scholar 

  • Kruidenier L, Kuiper I, Lamers CBHW, Verspaget HW (2003). Intestinal oxidative damage in inflammatory bowel disease: semi-quantification, localization, and association with mucosal antioxidants. J Pathol 201, 28–36.

    Article  CAS  PubMed  Google Scholar 

  • Lee DS, Evans JC, Robins SJ, Wilson PW, Albano I, Fox CS et al. (2007). Gamma glutamyl transferase and metabolic syndrome, cardiovascular disease, and mortality risk: the Framingham Heart Study. Arterioscler Thromb Vasc Biol 27, 127–133.

    Article  CAS  PubMed  Google Scholar 

  • Liou YA, King DJ, Zibrik D, Innis SM (2007). Decreasing linoleic acid with constant α-linolenic acid in dietary fats increases (n-3) eicosapentaenoic acid in plasma phospholipids in healthy men. J Nutr 137, 945–952.

    Article  CAS  PubMed  Google Scholar 

  • Ma TY (1997). Intestinal epithelial barrier dysfunction in Crohn's disease. Proc Soc Exp Biol Med 214, 318–327.

    Article  CAS  PubMed  Google Scholar 

  • Mann STW, Stracke H, Lange U, Klör HU, Teichmann J (2003). Vitamin D3 in patients with various grades of chronic pancreatitis, according to morphological and functional criteria of the pancreas. Dig Dis Sci 48, 533–538.

    Article  CAS  PubMed  Google Scholar 

  • Meisinger C, Döring A, Schneider A, Löwel H, for the KORA Study Group (2006). Serum γ-glutamyltransferase is a predictor of incident coronary events in apparently healthy men from the general population. Atherosclerosis 189, 297–302.

    Article  CAS  PubMed  Google Scholar 

  • Meister D, Ghosh S (2005). Effect of fish oil enriched enteral diet on inflammatory bowel disease tissues in organ culture: differential effects on ulcerative colitis and Crohn's disease. World J Gastroenterol 11, 7466–7472.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mills SC, Windsor AC, Knight SC (2005). The potential interactions between polyunsaturated fatty acids and colonic inflammatory processes. Clin Exp Immunol 142, 216–228.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mori TA (2004). Effect of fish and fish oil-derived omega-3 fatty acids on lipid oxidation. Redox Rep 9, 193–197.

    Article  CAS  PubMed  Google Scholar 

  • Morrow JD, Chen Y, Brame CJ, Yang J, Sanchez SC, Xu J et al. (1999). The isoprostanes: unique prostaglandin-like products of free-radical-initiated lipid peroxidation. Drug Metab Rev 31, 117–139.

    Article  CAS  PubMed  Google Scholar 

  • Nielsen AA, Jörgensen LGM, Nielsen JN, Eivindson M, Grönbaek H, Vind I et al. (2005). Omega-3 fatty acids inhibit an increase of proinflammatory cytokines in patients with active Crohn's disease compared with omega-6 fatty acids. Aliment Pharmacol Ther 22, 1121–1128.

    Article  CAS  PubMed  Google Scholar 

  • Peretti N, Roy CC, Drouin E, Seidman E, Brochu P, Casimir G et al. (2006). Abnormal intracellular lipid processing contributes to fat malabsorption in cystic fibrosis patients. Am J Physiol Gastrointest Liver Physiol 290, G609–G615.

    Article  CAS  PubMed  Google Scholar 

  • Periago JL, Suarez MD, Pita ML (1990). Effect of dietary olive oil, corn oil and medium-chain triglycerides on the lipid composition of rat red blood cell membranes. J Nutr 120, 986–994.

    Article  CAS  PubMed  Google Scholar 

  • Rantala AO, Lilja M, Kauma H, Savolainen MJ, Reunanen A, Kesäniemi YA (2000). Gamma-glutamyl transpeptidase and the metabolic syndrome. J Intern Med 248, 230–238.

    Article  CAS  PubMed  Google Scholar 

  • Romano C, Cucchiara S, Barabino A, Annese V, Sferlazzas C (2005). Usefulness of ω-3 fatty acid supplementation in addition to mesalazine in maintaining remission in pediatric Crohn's disease: a double-blind, randomized, placebo-controlled study. World J Gastroenterol 11, 7118–7121.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sabanayagam C, Shankar A, Li JL, Pollard C, Ducatman A (2009). Serum gamma-glutamyl transferase level and diabetes mellitus among US adults. Eur J Epidemiol 24, 369–373.

    Article  CAS  PubMed  Google Scholar 

  • Saito M, Kubo K (2003). Relationship between tissue lipid peroxidation and peroxidizability index after α-linolenic, eicosapentaenoic, or docosahexaenoic acid intake in rats. Br J Nutr 89, 19–28.

    Article  CAS  PubMed  Google Scholar 

  • Shankar A, Li J, Klein BEK, Nieto FJ, Klein R (2008). Serum gamma-glutamyltransferase level and peripheral arterial disease. Atherosclerosis 199, 102–109.

    Article  CAS  PubMed  Google Scholar 

  • Trebble TM, Arden NK, Wootton SA, Calder PC, Mullee MA, Fine DR et al. (2004). Fish oil and antioxidants alter the composition and function of circulating mononuclear cells in Crohn disease. Am J Clin Nutr 80, 1137–1144.

    Article  CAS  PubMed  Google Scholar 

  • Vuilleumier JP, Keller HE, Gysel D, Hunziker F (1983). Clinical chemical methods for the routine assessment of the vitamin status in human populations. Part I: the fat-soluble vitamins A and E, and beta-carotene. Int J Vitam Nutr Res 53, 265–272.

    CAS  PubMed  Google Scholar 

  • Whitfield JB (2001). Gamma glutamyl transferase. Crit Rev Clin Lab Sci 38, 263–355.

    Article  CAS  PubMed  Google Scholar 

  • Whiting CV, Bland PW, Tarlton JF (2005). Dietary n-3 polyunsaturated fatty acids reduce disease and colonic proinflammatory cytokines in a mouse model of colitis. Inflamm Bowel Dis 11, 340–349.

    Article  PubMed  Google Scholar 

  • Zhao S, Jia L, Gao P, Li Q, Lu X, Li J et al. (2008). Study on the effect of eicosapentaenoic acid on phospholipids composition in membrane microdomains of tight junctions of epithelial cells by liquid chromatography/electrospray mass spectrometry. J Pharm Biomed Anal 47, 343–350.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

CM coordinated the study and acted as an expert on fatty acid metabolism; RS conducted the study; RS and CM constituted the writing group and prepared this paper; BA and PS set up and performed the laboratory method of analysis of erythrocyte membrane fatty acids, plasma fat-soluble vitamins and 8-isoprostanes; BT was responsible for patient inclusion; BJ contributed to the collection of dietary and biochemical data; and NB conducted the statistical analysis. This study was supported in part by a research grant from Meduna Ltd, Isernhagen, Germany. Professor Metzner was a consultant for Meduna Ltd, Isernhagen, Germany. All authors contributed to the final version of the paper and gave their approval to publish the final version.

Author information

Authors and Affiliations

  1. Department of Urology, Medical Nutrition Science, University of Bonn, Bonn, Germany

    R Siener

  2. Department of Nutrition and Food Sciences, Nutritional Physiology, University of Bonn, Bonn, Germany

    B Alteheld & P Stehle

  3. Department of Internal Medicine I, University of Bonn, Bonn, Germany

    B Terjung

  4. Bonn Education Association for Dietetics r. A., Aachen, Germany

    B Junghans & C Metzner

  5. Department of Biostatistics,

    N Bitterlich

  6. Medicine and Service Ltd, Chemnitz, Germany

    N Bitterlich

  7. Department of Internal Medicine III, University Hospital, RWTH, Aachen, Germany

    C Metzner

Authors
  1. R Siener
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B Alteheld
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. B Terjung
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. B Junghans
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. N Bitterlich
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. P Stehle
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. C Metzner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to R Siener.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Siener, R., Alteheld, B., Terjung, B. et al. Change in the fatty acid pattern of erythrocyte membrane phospholipids after oral supplementation of specific fatty acids in patients with gastrointestinal diseases. Eur J Clin Nutr 64, 410–418 (2010). https://doi.org/10.1038/ejcn.2009.151

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ejcn.2009.151

Keywords

Search

Advanced search

Quick links