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

Atherosclerosis

Volumn 240, Issue 2, 2015, Pages 431-436

  Fontes, João D ^a,b   Rahman, Faisal ^c   Lacey, Sean ^a   Larson, Martin G ^a,d,e   Vasan, Ramachandran S ^a,b,e   Benjamin, Emelia J ^a,b,e   Harris, William S ^f   Robins, Sander J ^a,b  

^a FRAMINGHAM HEART STUDY   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c BOSTON UNIVERSITY MEDICAL CENTER   (United States)

^d USA   (United States)

^e BOSTON UNIVERSITY SCHOOL OF PUBLIC HEALTH   (United States)

^f UNIVERSITY OF SOUTH DAKOTA   (United States)

Author keywords

Biomarkers; Cross sectional study; Inflammation; Omega 3 fatty acids

Indexed keywords

1 ALKYL 2 ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE; BIOLOGICAL MARKER; C REACTIVE PROTEIN; DOCOSAHEXAENOIC ACID; FATTY ACID; ICOSAPENTAENOIC ACID; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; ISOPROSTANE DERIVATIVE; MONOCYTE CHEMOTACTIC PROTEIN 1; OMEGA 3 FATTY ACID; OSTEOPROTEGERIN; PADGEM PROTEIN; POLYUNSATURATED FATTY ACID; TUMOR NECROSIS FACTOR RECEPTOR 2; ANTIINFLAMMATORY AGENT; AUTACOID;

AGED; ARTICLE; BLOOD PRESSURE; ERYTHROCYTE; FEMALE; FRAMINGHAM RISK SCORE; HUMAN; INFLAMMATION; LIPID BLOOD LEVEL; LIPID COMPOSITION; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROGENY; BLOOD; CROSS-SECTIONAL STUDY; IMMUNOLOGY; MIDDLE AGED; MULTIVARIATE ANALYSIS; PROTECTION; RISK FACTOR;

AGED; ANTI-INFLAMMATORY AGENTS; BIOMARKERS; CROSS-SECTIONAL STUDIES; DOCOSAHEXAENOIC ACIDS; EICOSAPENTAENOIC ACID; ERYTHROCYTES; FEMALE; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; MALE; MIDDLE AGED; MULTIVARIATE ANALYSIS; PROTECTIVE FACTORS; RISK FACTORS;

EID: 84927778026     PISSN: 00219150     EISSN: 18791484     Source Type: Journal    
DOI: 10.1016/j.atherosclerosis.2015.03.043     Document Type: Article

References (65)

1. 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.
2. 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.
3. Larsson S.C., Orsini N. Fish consumption and the risk of stroke: a dose-response meta-analysis. Stroke 2011, 42:3621-3623.
4. 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.
5. 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.
6. 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.
7. 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.
8. Frostegard J. Immunity, atherosclerosis and cardiovascular disease. BMC Med. 2013, 11:117.
9. Libby P., Ridker P.M., Maseri A. Inflammation and atherosclerosis. Circulation 2002, 105:1135-1143.
10. 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.
11. Fontes J.D., Yamamoto J.F., Larson M.G., Wang N., Dallmeier D., Rienstra M., Schnabel R.B., Vasan R.S., Keaney J.F., Benjamin E.J. Clinical correlates of change in inflammatory biomarkers: the Framingham heart study. Atherosclerosis 2013, 228:217-223.
12. 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.
13. 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.
14. Kaysen G.A. The microinflammatory state in uremia: causes and potential consequences. J.Am. Soc. Nephrol. 2001, 12:1549-1557.
15. 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.
16. 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.
17. 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.
18. Harris W.S., Thomas R.M. Biological variability of blood omega-3 biomarkers. Clin. Biochem. 2010, 43:338-340.
19. Harris W.S. The omega-3 index: clinical utility for therapeutic intervention. Curr. Cardiol. Rep. 2010, 12:503-508.
20. 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.
21. Splansky G.L., Corey D., Yang Q., Atwood L.D., Cupples L.A., Benjamin E.J., D'Agostino 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.
22. 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.
23. 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.
24. 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.
25. 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 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.
26. 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.
27. 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.
28. 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.
29. 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.
30. 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.
31. 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.
32. 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.
33. 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.
34. 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.
35. 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.
36. Kishimoto T. Interleukin-6: from basic science to medicine-40 years in immunology. Annu Rev. Immunol. 2005, 23:1-21.
37. Keystone E.C., Ware C.F. Tumor necrosis factor and anti-tumor necrosis factor therapies. J.Rheumatol. Suppl. 2010, 85:27-39.
38. 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.
39. 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.
40. Kolattukudy P.E., Niu J. Inflammation, endoplasmic reticulum stress, autophagy, and the monocyte chemoattractant protein-1/ccr2 pathway. Circ. Res. 2012, 110:174-189.
41. Hua S. Targeting sites of inflammation: Intercellular adhesion molecule-1 as a target for novel inflammatory therapies. Front. Pharmacol. 2013, 4:127.
42. 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.
43. Calder P.C. Polyunsaturated fatty acids, inflammatory processes and inflammatory bowel diseases. Mol. Nutr. Food Res. 2008, 52:885-897.
44. Wong K.W. Clinical efficacy of n-3 fatty acid supplementation in patients with asthma. J.Am. Diet. Assoc. 2005, 105:98-105.
45. 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.
46. Adkins Y., Kelley D.S. Mechanisms underlying the cardioprotective effects of omega-3 polyunsaturated fatty acids. J.Nutr. Biochem. 2010, 21:781-792.
47. Calder P.C. Omega-3 polyunsaturated fatty acids and inflammatory processes: nutrition or pharmacology?. Br. J. Clin. Pharmacol. 2013, 75:645-662.
48. 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.
49. 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.
50. 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.
51. 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.
52. 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.
53. 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.
54. 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.
55. 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.
56. 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.
57. 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.
58. 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.
59. 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.
60. 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.
61. 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.
62. 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. 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. Group EJS.
63. 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.
64. 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.
65. 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.