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Epidemiology

Plasma omega-3 and saturated fatty acids are differentially related to pericardial adipose tissue volume across race/ethnicity: the Multi-ethnic Study of Atherosclerosis

Abstract

Background

Pericardial adipose tissue (PAT) is a cardiometabolic risk factor influenced by race/ethnicity, inflammation, and metabolic dysfunction. Omega-3 fatty acids (FAs) and saturated FAs (SFAs) are known to affect these latter phenomena and may influence PAT accumulation. We aimed to determine whether plasma levels of these FAs are related to PAT volume and its rate of change over a median 3-year follow-up.

Methods

Cardiac computed tomography assessed PAT in 6785 Multi-Ethnic Study of Atherosclerosis participants. Gas chromatography flame-ionization estimated plasma phospholipid FAs. Regression analyses estimated associations of FAs with PAT volume and its rate of change with adjustments for other risk factors. Race-interactions were tested.

Results

In cross-section, top tertiles of omega-3 FAs and odd-chained SFAs were associated with 2.8 and 4.93 cm3 lower PAT volumes, respectively; race/ethnicity was a significant modifying variable (p < 0.002). Even-chained SFAs were associated with 3.5 cm3 greater PAT volume. With stratification by race/ethnicity, Chinese Americans in the top tertile of omega-3 FAs showed 10.5 cm3 greater PAT volume than those in the referent tertile. Black individuals in the top tertile of odd-chained SFAs showed 5.0 cm3 lower PAT compared to referents. Black and Chinese Americans in top tertiles of even-chained SFAs showed respective 3.7 and 5.9 cm3 greater PAT volumes compared to referents. Two associations were observed in prospective analyses among Caucasians; race interactions were non-significant.

Conclusions

Cross-sectional and prospective findings provide inconclusive evidence as to whether plasma FAs are related to PAT in healthy individuals. Cohort studies with longer follow-up periods are warranted.

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References

  1. Iacobellis G. Epicardial and pericardial fat: close, but very different. Obes (Silver Spring). 2009;17:625.

    Article  Google Scholar 

  2. McClain J, Hsu F, Brown E, Burke G, Carr J, Harris T, et al. Pericardial adipose tissue and coronary artery calcification in the multi-ethnic study of atherosclerosis (MESA). Obes (Silver Spring). 2013;21:1056–63.

    Article  Google Scholar 

  3. Thanassoulis G, Massaro JM, O’Donnell CJ, Hoffmann U, Levy D, Ellinor PT, et al. Pericardial fat is associated with prevalent atrial fibrillation: the Framingham Heart Study. Circ Arrhythm Electrophysiol. 2010;3:345–50.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Al Chekakie MO, Welles CC, Metoyer R, Ibrahim A, Shapira AR, Cytron J, et al. Pericardial fat is independently associated with human atrial fibrillation. J Am Coll Cardiol. 2010;56:784–8.

    Article  PubMed  Google Scholar 

  5. Ding J, Hsu FC, Harris TB, Liu Y, Kritchevsky SB, Szklo M, et al. The association of pericardial fat with incident coronary heart disease: the Multi-Ethnic Study of Atherosclerosis (MESA). Am J Clin Nutr. 2009;90:499–504.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Yang FS, Yun CH, Wu TH, Hsieh YC, Bezerra HG, Liu CC, et al. High pericardial and peri-aortic adipose tissue burden in pre-diabetic and diabetic subjects. BMC Cardiovasc Disord. 2013;13:98.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Tadros TM, Massaro JM, Rosito GA, Hoffmann U, Vasan RS, Larson MG, et al. Pericardial fat volume correlates with inflammatory markers: the Framingham Heart Study. Obes (Silver Spring). 2010;18:1039–45.

    Article  Google Scholar 

  8. Bosy-Westphal A, Kossel E, Goele K, Blöcker T, Lagerpusch M, Later W. et al. Association of pericardial fat with liver fat and insulin sensitivity after diet-induced weight loss in overweight women. Obesity (Silver Spring). 2010;18:2111–7.

    Article  CAS  Google Scholar 

  9. Thanassoulis G, Massaro JM, Hoffmann U, Mahabadi AA, Vasan RS, O’Donnell CJ, et al. Prevalence, distribution, and risk factor correlates of high pericardial and intrathoracic fat depots in the Framingham heart study. Circ Cardiovasc Imaging. 2010;3:559–66.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Wei MY, Jacobson TA. Effects of eicosapentaenoic acid versus docosahexaenoic acid on serum lipids: a systematic review and meta-analysis. Curr Atheroscler Rep. 2011;13:474–83.

    Article  CAS  PubMed  Google Scholar 

  11. Neuhofer A, Zeyda M, Mascher D, Itariu BK, Murano I, Leitner L, et al. Impaired local production of proresolving lipid mediators in obesity and 17-HDHA as a potential treatment for obesity-associated inflammation. Diabetes 2013;62:1945–56.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Hellmann J, Tang Y, Kosuri M, Bhatnagar A, Spite M. Resolvin D1 decreases adipose tissue macrophage accumulation and improves insulin sensitivity in obese-diabetic mice. FASEB J. 2011;25:2399–407.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Popp-Snijders C, Schouten JA, Heine RJ, van der Meer J, van der Veen EA. Dietary supplementation of omega-3 polyunsaturated fatty acids improves insulin sensitivity in non-insulin-dependent diabetes. Diabetes Res. 1987;4:141–7.

    CAS  PubMed  Google Scholar 

  14. Gingras AA, White PJ, Chouinard PY, Julien P, Davis TA, Dombrowski L, et al. Long-chain omega-3 fatty acids regulate bovine whole-body protein metabolism by promoting muscle insulin signaling to the Akt-mTOR-S6K1 pathway and insulin sensitivity. J Physiol. 2007;579:269–84.

    Article  CAS  PubMed  Google Scholar 

  15. Sato T, Kameyama T, Ohori T, Matsuki A, Inoue H. Effects of eicosapentaenoic acid treatment on epicardial and abdominal visceral adipose tissue volumes in patients with coronary artery disease. J Atheroscler Thromb. 2014;21:1031–43.

    Article  CAS  PubMed  Google Scholar 

  16. Pacifico L, Bonci E, Di Martino M, Versacci P, Andreoli G, Silvestri LM, et al. A double-blind, placebo-controlled randomized trial to evaluate the efficacy of docosahexaenoic acid supplementation on hepatic fat and associated cardiovascular risk factors in overweight children with nonalcoholic fatty liver disease. Nutr Metab Cardiovasc Dis. 2015;25:734–41.

    Article  CAS  PubMed  Google Scholar 

  17. Ma W, Wu JH, Wang Q, Lemaitre RN, Mukamal KJ, Djoussé L, et al. Prospective association of fatty acids in the de novo lipogenesis pathway with risk of type 2 diabetes: the Cardiovascular Health Study. Am J Clin Nutr. 2015;101:153–63.

    Article  CAS  PubMed  Google Scholar 

  18. Zheng JS, Sharp SJ, Imamura F, Koulman A, Schulze MB, Ye Z, et al. Association between plasma phospholipid saturated fatty acids and metabolic markers of lipid, hepatic, inflammation and glycaemic pathways in eight European countries: a cross-sectional analysis in the EPIC-InterAct study. BMC Med. 2017;15:203.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Forouhi NG, Koulman A, Sharp SJ, Imamura F, Kröger J, Schulze MB, et al. Differences in the prospective association between individual plasma phospholipid saturated fatty acids and incident type 2 diabetes: the EPIC-InterAct case-cohort study. Lancet Diabetes Endocrinol. 2014;2:810–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Santaren ID, Watkins SM, Liese AD, Wagenknecht LE, Rewers MJ, Haffner SM, et al. Serum pentadecanoic acid (15:0), a short-term marker of dairy food intake, is inversely associated with incident type 2 diabetes and its underlying disorders. Am J Clin Nutr. 2014;100:1532–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Hodge AM, English DR, O’Dea K, Sinclair AJ, Makrides M, Gibson RA, et al. Plasma phospholipid and dietary fatty acids as predictors of type 2 diabetes: interpreting the role of linoleic acid. Am J Clin Nutr. 2007;86:189–97.

    Article  CAS  PubMed  Google Scholar 

  22. Steffen BT, Steffen LM, Tracy R, Siscovick D, Jacobs D, Liu K, et al. Ethnicity, plasma phospholipid fatty acid composition and inflammatory/endothelial activation biomarkers in the Multi-Ethnic Study of Atherosclerosis (MESA). Eur J Clin Nutr. 2012;66:600–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Lohner S, Fekete K, Marosvölgyi T, Decsi T. Gender differences in the long-chain polyunsaturated fatty acid status: systematic review of 51 publications. Ann Nutr Metab. 2013;62:98–112.

    Article  CAS  PubMed  Google Scholar 

  24. Bild DE, Bluemke DA, Burke GL, Detrano R, Diez Roux AV, Folsom AR, et al. Multi-Ethnic Study of Atherosclerosis: objectives and design. Am J Epidemiol. 2002;156:871–81.

    Article  PubMed  Google Scholar 

  25. Mackey RH, Greenland P, Goff DC Jr, Lloyd-Jones D, Sibley CT, Mora S. High-density lipoprotein cholesterol and particle concentrations, carotid atherosclerosis, and coronary events: MESA (multi-ethnic study of atherosclerosis). J Am Coll Cardiol. 2012;60:508–16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Tsai MY, Johnson C, Kao WH, Sharrett AR, Arends VL, Kronmal R, et al. Cholesteryl ester transfer protein genetic polymorphisms, HDL cholesterol, and subclinical cardiovascular disease in the multi-ethnic study of atherosclerosis. Atherosclerosis. 2008;200:359–67.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Cao J, Schwichtenberg KA, Hanson NQ, Tsai MY. Incorporation and clearance of omega-3 fatty acids in erythrocyte membranes and plasma phospholipids. Clin Chem. 2006;52:2265–72.

    Article  CAS  PubMed  Google Scholar 

  28. Ruzickova J, Rossmeisl M, Prazak T, Flachs P, Sponarova J, Veck M, et al. Omega-3 PUFA of marine origin limit diet-induced obesity in mice by reducing cellularity of adipose tissue. Lipids. 2004;39:1177–85.

    Article  CAS  PubMed  Google Scholar 

  29. Kim HK, Della-Fera M, Lin J, Baile CA. Docosahexae-noic acid inhibits adipocyte differentiation and induces apoptosis in 3T3-L1 preadipocytes. J Nutr. 2006;136:2965–9.

    Article  CAS  PubMed  Google Scholar 

  30. Satoh-Asahara N, Shimatsu A, Sasaki Y, Nakaoka H, Himeno A, Tochiya M, et al. Highly purified eicosapentaenoic acid increases interleukin-10 levels of peripheral blood monocytes in obese patients with dyslipidemia. Diabetes Care. 2012;35:2631–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Neschen S, Morino K, Dong J, Wang-Fischer Y, Cline GW, Romanelli AJ, et al. n-3 Fatty acids preserve insulin sensitivity in vivo in a peroxisome prolif-erator-activated receptor-alpha-dependent manner. Diabetes. 2007;56:1034–41.

    Article  CAS  PubMed  Google Scholar 

  32. Kadowaki T, Yamauchi T. Adiponectin and adiponectin receptors. Endocr Rev. 2005;26:439–51.

    Article  CAS  PubMed  Google Scholar 

  33. Sekikawa A, Miura K, Lee S, Fujiyoshi A, Edmundowicz D, Kadowaki T, et al. Long chain n-3 polyunsaturated fatty acids and incidence rate of coronary artery calcification in Japanese men in Japan and white men in the USA: population based prospective cohort study. Heart. 2014;100:569–73.

    Article  CAS  PubMed  Google Scholar 

  34. Suganami T, Tanimoto-Koyama K, Nishida J, Itoh M, Yuan X, Mizuarai S, et al. Role of the Toll-like receptor 4/NF-kappaB pathway in saturated fatty acid-induced inflammatory changes in the interaction between adipocytes and macrophages. Arterioscler Thromb Vasc Biol. 2007;27:84–91.

    Article  CAS  PubMed  Google Scholar 

  35. Chavez JA, Summers SA. Characterizing the effects of saturated fatty acids on insulin signaling and ceramide and diacylglycerol accumulation in 3T3-L1 adipocytes and C2C12 myotubes. Arch Biochem Biophys. 2003;419:101–9.

    Article  CAS  PubMed  Google Scholar 

  36. Wang Z, Liu D, Wang F, Liu S, Zhao S, Ling EA, et al. Saturated fatty acids activate microglia via Toll-like receptor 4/NF-kappaB signalling. Br J Nutr. 2012;107:229–41.

    Article  CAS  PubMed  Google Scholar 

  37. Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS. TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest. 2006;116:3015–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Steffen BT, Duprez D, Szklo M, Guan W, Tsai MY. Circulating oleic acid levels are related to greater risks of cardiovascular events and all-cause mortality: the multi-ethnic study of atherosclerosis. J Clin Lipido. 2018;12:1404–12.

    Article  Google Scholar 

  39. Ma J, Folsom AR, Shahar E, Eckfeldt JH. Plasma fatty acid composition as an indicator of habitual dietary fat intake in middle-aged adults. Am J Clin Nutr. 1995;62:564–71.

    Article  CAS  PubMed  Google Scholar 

  40. Forsythe CE, Phinney SD, Fernandez ML, Quann EE, Wood RJ, Bibus DM, et al. Comparison of low fat and low carbohydrate diets on circulating fatty acid composition and markers of inflammation. Lipids. 2008;43:65–77.

    Article  CAS  PubMed  Google Scholar 

  41. Forsythe CE, Phinney SD, Feinman RD, Volk BM, Freidenreich D, Quann E, et al. Limited effect of dietary saturated fat on plasma saturated fat in the context of a low carbohydrate diet. Lipids. 2010;45:947–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank the other investigators, the staff, and the participants of the MESA study for their valuable contributions. A full list of participating MESA investigators and institutions can be found at http://www.mesa-nhlbi.org.

Funding

This research was supported by contracts HHSN268201500003I, N01-HC-95159, N01-HC-95160, N01-HC-95161, N01-HC-95162, N01-HC-95163, N01-HC-95164, N01-HC-95165, N01-HC-95166, N01-HC-95167, N01-HC-95168 and N01-HC-95169 from the National Heart, Lung, and Blood Institute, and by grants UL1-TR-000040, UL1-TR-001079, and UL1-TR-001420 from NCATS.

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Correspondence to Michael Y. Tsai.

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Steffen, B.T., Guan, W., Ding, J. et al. Plasma omega-3 and saturated fatty acids are differentially related to pericardial adipose tissue volume across race/ethnicity: the Multi-ethnic Study of Atherosclerosis. Eur J Clin Nutr 75, 1237–1244 (2021). https://doi.org/10.1038/s41430-020-00833-x

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