Advertisement
Research Article| Volume 240, ISSUE 2, P431-436, June 2015

Download started.

Ok

Red blood cell fatty acids and biomarkers of inflammation: A cross-sectional study in a community-based cohort

  • Author Footnotes
    1 First authors.
    João D. Fontes
    Footnotes
    1 First authors.
    Affiliations
    National Heart Lung and Blood Institute's and Boston University's Framingham Heart Study, Framingham, MA, USA

    Department of Cardiology and Preventive Medicine, Boston University School of Medicine, Boston, MA, USA

    Department of Medicine, Boston University School of Medicine, Boston, MA, USA
    Search for articles by this author
  • Author Footnotes
    1 First authors.
    Faisal Rahman
    Footnotes
    1 First authors.
    Affiliations
    Boston University Medical Center, Boston, MA 02118, USA
    Search for articles by this author
  • Sean Lacey
    Affiliations
    National Heart Lung and Blood Institute's and Boston University's Framingham Heart Study, Framingham, MA, USA
    Search for articles by this author
  • Martin G. Larson
    Affiliations
    National Heart Lung and Blood Institute's and Boston University's Framingham Heart Study, Framingham, MA, USA

    Department of Mathematics and Statistics, Boston University, Boston, MA, USA

    Department of Biostatistics, Boston University School of Public Health, Boston, MA, USA
    Search for articles by this author
  • Ramachandran S. Vasan
    Affiliations
    National Heart Lung and Blood Institute's and Boston University's Framingham Heart Study, Framingham, MA, USA

    Department of Cardiology and Preventive Medicine, Boston University School of Medicine, Boston, MA, USA

    Department of Medicine, Boston University School of Medicine, Boston, MA, USA

    Epidemiology Department, Boston University School of Public Health, Boston, MA, USA
    Search for articles by this author
  • Emelia J. Benjamin
    Affiliations
    National Heart Lung and Blood Institute's and Boston University's Framingham Heart Study, Framingham, MA, USA

    Department of Cardiology and Preventive Medicine, Boston University School of Medicine, Boston, MA, USA

    Department of Medicine, Boston University School of Medicine, Boston, MA, USA

    Epidemiology Department, Boston University School of Public Health, Boston, MA, USA
    Search for articles by this author
  • William S. Harris
    Correspondence
    Corresponding author.
    Affiliations
    Department of Medicine, Sanford School of Medicine, University of South Dakota, and OmegaQuant Analytics, LLC, 5009 W. 12th St, Ste 8, Sioux Falls, SD 57106, USA
    Search for articles by this author
  • Sander J. Robins
    Affiliations
    National Heart Lung and Blood Institute's and Boston University's Framingham Heart Study, Framingham, MA, USA

    Department of Cardiology and Preventive Medicine, Boston University School of Medicine, Boston, MA, USA

    Department of Medicine, Boston University School of Medicine, Boston, MA, USA
    Search for articles by this author
  • Author Footnotes
    1 First authors.

      Highlights

      • RBC omega-3 FAs were compared with 10 inflammatory biomarkers in 2724 subjects.
      • RBC FA levels are less affected by daily variations in intake than plasma FA levels.
      • 8 out of 10 biomarkers were inversely associated with omega-3 levels.
      • These findings suggest that omega-3 FA may have anti-inflammatory properties.

      Abstract

      Introduction

      Inflammation and inflammatory biomarkers have emerged as integral components and predictors of incident cardiovascular (CV) disease. Omega-3 fatty acids, particularly eicosapentaenoic and docosahexaenoic acids (EPA and DHA) have anti-inflammatory properties, and have been variably associated with lower blood pressure, favorable blood lipid changes, and reduced CV events.

      Methods and results

      We examined the cross-sectional association of red blood cell (RBC) fatty acids, representative of body membrane fatty acid composition, with 10 biomarkers active in multiple inflammatory pathways in 2724 participants (mean age 66 ± 9 years, 54% women, 8% minorities) from the Framingham Offspring and minority Omni Cohorts. After multivariable adjustment, the RBC EPA and DHA content was inversely correlated (all P ≤ 0.001) with 8 biomarkers: urinary isoprostanes (r = −0.16); and soluble interleukin-6 (r = −0.10); C-reactive protein (r = −0.08); tumor necrosis factor receptor 2 (r = −0.08); intercellular adhesion molecule-1 (r = −0.08); P-selectin (r = −0.06); lipoprotein-associated phospholipase-A2 mass (r = −0.11) and activity (r = −0.08). The correlations for monocyte chemoattractant protein-1 was −0.05, P = 0.006 and osteoprotegerin (r = −0.06, P = 0.002) were only nominally significant.

      Conclusion

      In our large community-based study, we observed modest inverse associations between several types of inflammatory biomarkers with RBC omega-3 fatty acid levels. Our findings are consistent with the hypothesis that omega-3 fatty acids have anti-inflammatory properties.

      Keywords

      Abbreviations:

      RBC (red blood cell), PUFA (polyunsaturated fatty acid(s)), EPA (eicosapentaenoic acid), DHA (docosahexaenoic acid)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Atherosclerosis
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Zheng J.
        • Huang T.
        • Yu Y.
        • Hu X.
        • Yang B.
        • Li D.
        Fish consumption and chd mortality: an updated meta-analysis of seventeen cohort studies.
        Public Health Nutr. 2012; 15: 725-737
        • He K.
        • Song Y.
        • Daviglus M.L.
        • Liu K.
        • Van Horn L.
        • Dyer A.R.
        • Goldbourt U.
        • Greenland P.
        Fish consumption and incidence of stroke: a meta-analysis of cohort studies.
        Stroke. 2004; 35: 1538-1542
        • Larsson S.C.
        • Orsini N.
        Fish consumption and the risk of stroke: a dose-response meta-analysis.
        Stroke. 2011; 42: 3621-3623
        • Huang T.L.
        • Zandi P.P.
        • Tucker K.L.
        • Fitzpatrick A.L.
        • Kuller L.H.
        • Fried L.P.
        • Burke G.L.
        • Carlson M.C.
        Benefits of fatty fish on dementia risk are stronger for those without apoe epsilon4.
        Neurology. 2005; 65: 1409-1414
        • Albert C.M.
        • Campos H.
        • Stampfer M.J.
        • Ridker P.M.
        • Manson J.E.
        • Willett W.C.
        • Ma J.
        Blood levels of long-chain n-3 fatty acids and the risk of sudden death.
        N. Engl. J. Med. 2002; 346: 1113-1118
        • Wang C.
        • Harris W.S.
        • Chung M.
        • Lichtenstein A.H.
        • Balk E.M.
        • Kupelnick B.
        • Jordan H.S.
        • 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
        • Mozaffarian D.
        • Lemaitre R.N.
        • King I.B.
        • Song X.
        • Huang H.
        • Sacks F.M.
        • Rimm E.B.
        • Wang M.
        • Siscovick D.S.
        Plasma phospholipid long-chain omega-3 fatty acids and total and cause-specific mortality in older adults: a cohort study.
        Ann. Intern Med. 2013; 158: 515-525
        • Frostegard J.
        Immunity, atherosclerosis and cardiovascular disease.
        BMC Med. 2013; 11: 117
        • Libby P.
        • Ridker P.M.
        • Maseri A.
        Inflammation and atherosclerosis.
        Circulation. 2002; 105: 1135-1143
        • Wang T.J.
        • Gona P.
        • Larson M.G.
        • Levy D.
        • Benjamin E.J.
        • Tofler G.H.
        • Jacques P.F.
        • Meigs J.B.
        • Rifai N.
        • Selhub J.
        • Robins S.J.
        • Newton-Cheh C.
        • Vasan R.S.
        Multiple biomarkers and the risk of incident hypertension.
        Hypertension. 2007; 49: 432-438
        • Fontes J.D.
        • Yamamoto J.F.
        • Larson M.G.
        • Wang N.
        • Dallmeier D.
        • Rienstra M.
        • Schnabel R.B.
        • Vasan R.S.
        • Keaney Jr., J.F.
        • Benjamin E.J.
        Clinical correlates of change in inflammatory biomarkers: the Framingham heart study.
        Atherosclerosis. 2013; 228: 217-223
        • Mishra M.
        • Kumar H.
        • Bajpai S.
        • Singh R.K.
        • Tripathi K.
        Level of serum il-12 and its correlation with endothelial dysfunction, insulin resistance, proinflammatory cytokines and lipid profile in newly diagnosed type 2 diabetes.
        Diabetes Res. Clin. Pract. 2011; 94: 255-261
        • Conway D.S.
        • Buggins P.
        • Hughes E.
        • Lip G.Y.
        Relationship of interleukin-6 and c-reactive protein to the prothrombotic state in chronic atrial fibrillation.
        J. Am. Coll. Cardiol. 2004; 43: 2075-2082
        • Kaysen G.A.
        The microinflammatory state in uremia: causes and potential consequences.
        J. Am. Soc. Nephrol. 2001; 12: 1549-1557
        • Li K.
        • Huang T.
        • Zheng J.
        • Wu K.
        • Li D.
        Effect of marine-derived n-3 polyunsaturated fatty acids on c-reactive protein, interleukin 6 and tumor necrosis factor alpha: a meta-analysis.
        PLoS One. 2014; 9: e88103
        • Steffen B.T.
        • Steffen L.M.
        • Liang S.
        • Tracy R.
        • Jenny N.S.
        • Tsai M.Y.
        N-3 and n-6 fatty acids are independently associated with lipoprotein-associated phospholipase a2 in the multi-ethnic study of atherosclerosis.
        Br. J. Nutr. 2013; 110: 1664-1671
        • Steffen B.T.
        • Steffen L.M.
        • Tracy R.
        • Siscovick D.
        • Jacobs D.
        • Liu K.
        • He K.
        • Hanson N.Q.
        • Nettleton J.A.
        • Tsai M.Y.
        Ethnicity, plasma phospholipid fatty acid composition and inflammatory/endothelial activation biomarkers in the multi-ethnic study of atherosclerosis (mesa).
        Eur. J. Clin. Nutr. 2012; 66: 600-605
        • Harris W.S.
        • Thomas R.M.
        Biological variability of blood omega-3 biomarkers.
        Clin. Biochem. 2010; 43: 338-340
        • Harris W.S.
        The omega-3 index: clinical utility for therapeutic intervention.
        Curr. Cardiol. Rep. 2010; 12: 503-508
        • Kannel W.B.
        • Feinleib M.
        • McNamara P.M.
        • Garrison R.J.
        • Castelli W.P.
        An investigation of coronary heart disease in families. The Framingham offspring study.
        Am. J. Epidemiol. 1979; 110: 281-290
        • Splansky G.L.
        • Corey D.
        • Yang Q.
        • Atwood L.D.
        • Cupples L.A.
        • Benjamin E.J.
        • D'Agostino Sr., R.B.
        • Fox C.S.
        • Larson M.G.
        • Murabito J.M.
        • O'Donnell C.J.
        • Vasan R.S.
        • Wolf P.A.
        • Levy D.
        The third generation cohort of the national heart, lung, and blood institute's Framingham heart study: design, recruitment, and initial examination.
        Am. J. Epidemiol. 2007; 165: 1328-1335
        • Quan S.F.
        • Howard B.V.
        • Iber C.
        • Kiley J.P.
        • Nieto F.J.
        • O'Connor G.T.
        • Rapoport D.M.
        • Redline S.
        • Robbins J.
        • Samet J.M.
        • Wahl P.W.
        The sleep heart health study: design, rationale, and methods.
        Sleep. 1997; 20: 1077-1085
        • Harris W.S.
        • Pottala J.V.
        • Vasan R.S.
        • Larson M.G.
        • Robins S.J.
        Changes in erythrocyte membrane trans and marine fatty acids between 1999 and 2006 in older americans.
        J. Nutr. 2012; 142: 1297-1303
        • Harris W.S.
        • von Schacky C.
        The omega-3 index: a new risk factor for death from coronary heart disease?.
        Prev. Med. 2004; 39: 212-220
        • Schnabel R.
        • Larson M.G.
        • Dupuis J.
        • Lunetta K.L.
        • Lipinska I.
        • Meigs J.B.
        • Yin X.
        • Rong J.
        • Vita J.A.
        • Newton-Cheh C.
        • Levy D.
        • Keaney Jr., J.F.
        • Vasan R.S.
        • Mitchell G.F.
        • Benjamin E.J.
        Relations of inflammatory biomarkers and common genetic variants with arterial stiffness and wave reflection.
        Hypertension. 2008; 51: 1651-1657
        • Bays H.E.
        • Ballantyne C.M.
        • Braeckman R.A.
        • Stirtan W.G.
        • Soni P.N.
        Icosapent ethyl, a pure ethyl ester of eicosapentaenoic acid: effects on circulating markers of inflammation from the marine and anchor studies.
        Am. J. Cardiovasc. Drugs. 2013; 13: 37-46
        • Maki K.C.
        • Bays H.E.
        • Dicklin M.R.
        • Johnson S.L.
        • Shabbout M.
        Effects of prescription omega-3-acid ethyl esters, coadministered with atorvastatin, on circulating levels of lipoprotein particles, apolipoprotein ciii, and lipoprotein-associated phospholipase a2 mass in men and women with mixed dyslipidemia.
        J. Clin. Lipidol. 2011; 5: 483-492
        • Davidson M.H.
        • Maki K.C.
        • Bays H.
        • Carter R.
        • Ballantyne C.M.
        Effects of prescription omega-3-acid ethyl esters on lipoprotein particle concentrations, apolipoproteins ai and ciii, and lipoprotein-associated phospholipase a(2) mass in statin-treated subjects with hypertriglyceridemia.
        J. Clin. Lipidol. 2009; 3: 332-340
        • Massaro M.
        • Scoditti E.
        • Carluccio M.A.
        • Campana M.C.
        • De Caterina R.
        Omega-3 fatty acids, inflammation and angiogenesis: basic mechanisms behind the cardioprotective effects of fish and fish oils.
        Cell. Mol. Biol. (Noisy-le-grand). 2010; 56: 59-82
        • Draper E.
        • Reynolds C.M.
        • Canavan M.
        • Mills K.H.
        • Loscher C.E.
        • Roche H.M.
        Omega-3 fatty acids attenuate dendritic cell function via nf-κb independent of pparγ.
        J. Nutr. Biochem. 2011; 22: 784-790
        • Li H.
        • Ruan X.Z.
        • Powis S.H.
        • Fernando R.
        • Mon W.Y.
        • Wheeler D.C.
        • Moorhead J.F.
        • Varghese Z.
        Epa and dha reduce lps-induced inflammation responses in hk-2 cells: evidence for a ppar-γ–dependent mechanism.
        Kidney Int. 2005; 67: 867-874
        • Wang T.-M.
        • Hsieh S.-C.
        • Chen J.-W.
        • Chiang A.-N.
        Docosahexaenoic acid and eicosapentaenoic acid reduce c-reactive protein expression and stat3 activation in il-6-treated hepg2 cells.
        Mol. Cell. Biochem. 2013; 377: 97-106
        • Wada M.
        • DeLong C.J.
        • Hong Y.H.
        • Rieke C.J.
        • Song I.
        • Sidhu R.S.
        • Yuan C.
        • Warnock M.
        • Schmaier A.H.
        • Yokoyama C.
        • Smyth E.M.
        • Wilson S.J.
        • FitzGerald G.A.
        • Garavito R.M.
        • Sui de X.
        • Regan J.W.
        • Smith W.L.
        Enzymes and receptors of prostaglandin pathways with arachidonic acid-derived versus eicosapentaenoic acid-derived substrates and products.
        J. Biol. Chem. 2007; 282: 22254-22266
        • Bagga D.
        • Wang L.
        • Farias-Eisner R.
        • Glaspy J.A.
        • Reddy S.T.
        Differential effects of prostaglandin derived from omega-6 and omega-3 polyunsaturated fatty acids on cox-2 expression and il-6 secretion.
        Proc. Natl. Acad. Sci. U. S. A. 2003; 100: 1751-1756
        • Mullen A.
        • Loscher C.E.
        • Roche H.M.
        Anti-inflammatory effects of epa and dha are dependent upon time and dose-response elements associated with lps stimulation in thp-1-derived macrophages.
        J. Nutr. Biochem. 2010; 21: 444-450
        • Kishimoto T.
        Interleukin-6: from basic science to medicine–40 years in immunology.
        Annu Rev. Immunol. 2005; 23: 1-21
        • Keystone E.C.
        • Ware C.F.
        Tumor necrosis factor and anti-tumor necrosis factor therapies.
        J. Rheumatol. Suppl. 2010; 85: 27-39
        • Nishimoto N.
        • Terao K.
        • Mima T.
        • Nakahara H.
        • Takagi N.
        • Kakehi T.
        Mechanisms and pathologic significances in increase in serum interleukin-6 (il-6) and soluble il-6 receptor after administration of an anti-il-6 receptor antibody, tocilizumab, in patients with rheumatoid arthritis and castleman disease.
        Blood. 2008; 112: 3959-3964
        • Basu S.
        Bioactive eicosanoids: role of prostaglandin f(2alpha) and f(2)-isoprostanes in inflammation and oxidative stress related pathology.
        Mol. Cells. 2010; 30: 383-391
        • Kolattukudy P.E.
        • Niu J.
        Inflammation, endoplasmic reticulum stress, autophagy, and the monocyte chemoattractant protein-1/ccr2 pathway.
        Circ. Res. 2012; 110: 174-189
        • Hua S.
        Targeting sites of inflammation: Intercellular adhesion molecule-1 as a target for novel inflammatory therapies.
        Front. Pharmacol. 2013; 4: 127
        • Rosenson R.S.
        • Stafforini D.M.
        Modulation of oxidative stress, inflammation, and atherosclerosis by lipoprotein-associated phospholipase a2.
        J. Lipid Res. 2012; 53: 1767-1782
        • Calder P.C.
        Polyunsaturated fatty acids, inflammatory processes and inflammatory bowel diseases.
        Mol. Nutr. Food Res. 2008; 52: 885-897
        • Wong K.W.
        Clinical efficacy of n-3 fatty acid supplementation in patients with asthma.
        J. Am. Diet. Assoc. 2005; 105: 98-105
        • Lee Y.H.
        • Bae S.C.
        • Song G.G.
        Omega-3 polyunsaturated fatty acids and the treatment of rheumatoid arthritis: a meta-analysis.
        Arch. Med. Res. 2012; 43: 356-362
        • Adkins Y.
        • Kelley D.S.
        Mechanisms underlying the cardioprotective effects of omega-3 polyunsaturated fatty acids.
        J. Nutr. Biochem. 2010; 21: 781-792
        • Calder P.C.
        Omega-3 polyunsaturated fatty acids and inflammatory processes: nutrition or pharmacology?.
        Br. J. Clin. Pharmacol. 2013; 75: 645-662
        • Pischon T.
        • Hankinson S.E.
        • Hotamisligil G.S.
        • Rifai N.
        • Willett W.C.
        • Rimm E.B.
        Habitual dietary intake of n-3 and n-6 fatty acids in relation to inflammatory markers among us men and women.
        Circulation. 2003; 108: 155-160
        • He K.
        • Liu K.
        • Daviglus M.L.
        • Jenny N.S.
        • Mayer-Davis E.
        • Jiang R.
        • Steffen L.
        • Siscovick D.
        • Tsai M.
        • Herrington D.
        Associations of dietary long-chain n-3 polyunsaturated fatty acids and fish with biomarkers of inflammation and endothelial activation (from the multi-ethnic study of atherosclerosis [mesa]).
        Am. J. Cardiol. 2009; 103: 1238-1243
        • Lund A.S.
        • Hasselbalch A.L.
        • Gamborg M.
        • Skogstrand K.
        • Hougaard D.M.
        • Heitmann B.L.
        • Kyvik K.O.
        • Sorensen T.I.
        • Jess T.
        N-3 polyunsaturated fatty acids, body fat and inflammation.
        Obes. Facts. 2013; 6: 369-379
        • Niu K.
        • Hozawa A.
        • Kuriyama S.
        • Ohmori-Matsuda K.
        • Shimazu T.
        • Nakaya N.
        • Fujita K.
        • Tsuji I.
        • Nagatomi R.
        Dietary long-chain n-3 fatty acids of marine origin and serum c-reactive protein concentrations are associated in a population with a diet rich in marine products.
        Am. J. Clin. Nutr. 2006; 84: 223-229
        • Zampelas A.
        • Panagiotakos D.B.
        • Pitsavos C.
        • Das U.N.
        • Chrysohoou C.
        • Skoumas Y.
        • Stefanadis C.
        Fish consumption among healthy adults is associated with decreased levels of inflammatory markers related to cardiovascular disease: the Attica study.
        J. Am. Coll. Cardiol. 2005; 46: 120-124
        • Lopez-Garcia E.
        • Schulze M.B.
        • Manson J.E.
        • Meigs J.B.
        • Albert C.M.
        • Rifai N.
        • Willett W.C.
        • Hu F.B.
        Consumption of (n-3) fatty acids is related to plasma biomarkers of inflammation and endothelial activation in women.
        J. Nutr. 2004; 134: 1806-1811
        • Murakami K.
        • Sasaki S.
        • Takahashi Y.
        • Uenishi K.
        • Yamasaki M.
        • Hayabuchi H.
        • Goda T.
        • Oka J.
        • Baba K.
        • Ohki K.
        • Muramatsu K.
        • Sugiyama Y.
        Total n-3 polyunsaturated fatty acid intake is inversely associated with serum c-reactive protein in young japanese women.
        Nutr. Res. 2008; 28: 309-314
        • Poudel-Tandukar K.
        • Nanri A.
        • Matsushita Y.
        • Sasaki S.
        • Ohta M.
        • Sato M.
        • Mizoue T.
        Dietary intakes of alpha-linolenic and linoleic acids are inversely associated with serum c-reactive protein levels among Japanese men.
        Nutr. Res. 2009; 29: 363-370
        • Farzaneh-Far R.
        • Harris W.S.
        • Garg S.
        • Na B.
        • Whooley M.A.
        Inverse association of erythrocyte n-3 fatty acid levels with inflammatory biomarkers in patients with stable coronary artery disease: the heart and soul study.
        Atherosclerosis. 2009; 205: 538-543
        • Grenon S.M.
        • Conte M.S.
        • Nosova E.
        • Alley H.
        • Chong K.
        • Harris W.S.
        • Vittinghoff E.
        • Owens C.D.
        Association between n-3 polyunsaturated fatty acid content of red blood cells and inflammatory biomarkers in patients with peripheral artery disease.
        J. Vasc. Surg. 2013; 58: 1283-1290
        • Kalogeropoulos N.
        • Panagiotakos D.B.
        • Pitsavos C.
        • Chrysohoou C.
        • Rousinou G.
        • Toutouza M.
        • Stefanadis C.
        Unsaturated fatty acids are inversely associated and n-6/n-3 ratios are positively related to inflammation and coagulation markers in plasma of apparently healthy adults.
        Clin. Chim. Acta. 2010; 411: 584-591
        • Baek D.
        • Park Y.
        Association between erythrocyte n-3 polyunsaturated fatty acids and biomarkers of inflammation and oxidative stress in patients with and without depression.
        Prostagl. Leukot. Essent. Fat. Acids. 2013; 89: 291-296
        • Ferrucci L.
        • Cherubini A.
        • Bandinelli S.
        • Bartali B.
        • Corsi A.
        • Lauretani F.
        • Martin A.
        • Andres-Lacueva C.
        • Senin U.
        • Guralnik J.M.
        Relationship of plasma polyunsaturated fatty acids to circulating inflammatory markers.
        J. Clin. Endocrinol. Metab. 2006; 91: 439-446
        • Reinders I.
        • Virtanen J.K.
        • Brouwer I.A.
        • Tuomainen T.P.
        Association of serum n-3 polyunsaturated fatty acids with c-reactive protein in men.
        Eur. J. Clin. Nutr. 2012; 66: 736-741
        • Sekikawa A.
        • Kadowaki T.
        • Curb J.D.
        • Evans R.W.
        • Maegawa H.
        • Abbott R.D.
        • Sutton-Tyrrell K.
        • Okamura T.
        • Shin C.
        • Edmundowicz D.
        • Kadota A.
        • Choo J.
        • El-Saed A.
        • Ueshima H.
        • Kuller L.H.
        • Group EJS
        Circulating levels of 8 cytokines and marine n-3 fatty acids and indices of obesity in Japanese, white, and Japanese American middle-aged men.
        J. Interferon Cytokine Res. 2010; 30: 541-548
        • Micallef M.A.
        • Munro I.A.
        • Garg M.L.
        An inverse relationship between plasma n-3 fatty acids and c-reactive protein in healthy individuals.
        Eur. J. Clin. Nutr. 2009; 63: 1154-1156
        • Labonte M.E.
        • Dewailly E.
        • Lucas M.
        • Couture P.
        • Lamarche B.
        Association of red blood cell n-3 polyunsaturated fatty acids with plasma inflammatory biomarkers among the quebec cree population.
        Eur. J. Clin. Nutr. 2014;
        • Schmidt E.B.
        • Koenig W.
        • Khuseyinova N.
        • Christensen J.H.
        Lipoprotein-associated phospholipase a2 concentrations in plasma are associated with the extent of coronary artery disease and correlate to adipose tissue levels of marine n-3 fatty acids.
        Atherosclerosis. 2008; 196: 420-424