Lipids

, Volume 48, Issue 6, pp 557–567 | Cite as

Egg Consumption Modulates HDL Lipid Composition and Increases the Cholesterol-Accepting Capacity of Serum in Metabolic Syndrome

  • Catherine J. Andersen
  • Christopher N. Blesso
  • Jiyoung Lee
  • Jacqueline Barona
  • Dharika Shah
  • Michael J. Thomas
  • Maria Luz Fernandez
Original Article

Abstract

We recently demonstrated that daily whole egg consumption during moderate carbohydrate restriction leads to greater increases in plasma HDL-cholesterol (HDL-C) and improvements in HDL profiles in metabolic syndrome (MetS) when compared to intake of a yolk-free egg substitute. We further investigated the effects of this intervention on HDL composition and function, hypothesizing that the phospholipid species present in egg yolk modulate HDL lipid composition to increase the cholesterol-accepting capacity of subject serum. Men and women classified with MetS were randomly assigned to consume either three whole eggs (EGG, n = 20) per day or the equivalent amount of egg substitute (SUB, n = 17) throughout a 12-week moderate carbohydrate-restricted (25–30 % of energy) diet. Relative to other HDL lipids, HDL-cholesteryl ester content increased in all subjects, with greater increases in the SUB group. Further, HDL-triacylglycerol content was reduced in EGG group subjects with normal baseline plasma HDL-C, resulting in increases in HDL-CE/TAG ratios in both groups. Phospholipid analysis by mass spectrometry revealed that HDL became enriched in phosphatidylethanolamine in the EGG group, and that EGG group HDL better reflected sphingomyelin species present in the whole egg product at week 12 compared to baseline. Further, macrophage cholesterol efflux to EGG subject serum increased from baseline to week 12, whereas no changes were observed in the SUB group. Together, these findings suggest that daily egg consumption promotes favorable shifts in HDL lipid composition and function beyond increasing plasma HDL-C in MetS.

Keywords

HDL Phospholipids Cholesterol efflux Metabolic syndrome Eggs Carbohydrate-restricted diet 

Abbreviations

ABCA1

ATP-binding cassette transporter A1

ABCG1

ATP-binding cassette transporter G1

BCA

Bicinchoninic acid

CAD

Coronary artery disease

CE

Cholesteryl ester

CerPCho

Sphingomyelin

CETP

Cholesteryl ester transfer protein

CVD

Cardiovascular disease

DMPC

Dimyristoylphosphatidylcholine

EGG

Whole egg group

FC

Free cholesterol

HDL-C

Plasma HDL-cholesterol

HDL-PL

HDL-phospholipids

LCAT

Lecithin-cholesterol acyltransferase

LysoPtdCho

Lysophosphatidylcholine

NCEP ATP III

National Cholesterol Education Program Adult Treatment Panel III

MetS

Metabolic syndrome

PL

Phospholipid

PtdCho

Phosphatidylcholine

PtdEtn

Phosphatidylethanolamine

PtdIns

Phosphatidylinositol

RCT

Reverse cholesterol transport

SDS

Sodium dodecyl sulfate

SR-BI

Scavenger receptor class B I

SUB

Egg yolk-free egg substitute group

TAG

Triacylglycerol

References

  1. 1.
    Cornier MA, Dabelea D, Hernandez TL, Lindstrom RC, Steig AJ, Stob NR, Van Pelt RE, Wang H, Eckel RH (2008) The metabolic syndrome. Endocr Rev 29:777–822PubMedCrossRefGoogle Scholar
  2. 2.
    Rader DJ, Alexander ET, Weibel GL, Billheimer J, Rothblat GH (2009) The role of reverse cholesterol transport in animals and humans and relationship to atherosclerosis. J Lipid Res 50(Suppl):S189–S194PubMedGoogle Scholar
  3. 3.
    Asztalos BF, Tani M, Schaefer EJ (2011) Metabolic and functional relevance of HDL subspecies. Curr Opin Lipidol 22:176–185PubMedCrossRefGoogle Scholar
  4. 4.
    Barter PJ, Nicholls S, Rye KA, Anantharamaiah GM, Navab M, Fogelman AM (2004) Antiinflammatory properties of HDL. Circ Res 95:764–772PubMedCrossRefGoogle Scholar
  5. 5.
    Khera AV, Cuchel M, de la Llera-Moya M, Rodrigues A, Burke MF, Jafri K, French BC, Phillips JA, Mucksavage ML, Wilensky RL, Mohler ER, Rothblat GH, Rader DJ (2011) Cholesterol efflux capacity, high-density lipoprotein function, and atherosclerosis. N Engl J Med 364:127–135PubMedCrossRefGoogle Scholar
  6. 6.
    Kontush A, Chapman MJ (2006) Functionally defective high-density lipoprotein: a new therapeutic target at the crossroads of dyslipidemia, inflammation, and atherosclerosis. Pharmacol Rev 58:342–374PubMedCrossRefGoogle Scholar
  7. 7.
    Tchoua U, Gillard BK, Pownall HJ (2010) HDL superphospholipidation enhances key steps in reverse cholesterol transport. Atherosclerosis 209:430–435PubMedCrossRefGoogle Scholar
  8. 8.
    Fournier N, Paul JL, Atger V, Cogny A, Soni T, de la Llera-Moya M, Rothblat G, Moatti N (1997) HDL phospholipid content and composition as a major factor determining cholesterol efflux capacity from Fu5AH cells to human serum. Arterioscler Thromb Vasc Biol 17:2685–2691PubMedCrossRefGoogle Scholar
  9. 9.
    Rosenson RS, Brewer HB Jr, Chapman MJ, Fazio S, Hussain MM, Kontush A, Krauss RM, Otvos JD, Remaley AT, Schaefer EJ (2011) HDL measures, particle heterogeneity, proposed nomenclature, and relation to atherosclerotic cardiovascular events. Clin Chem 57:392–410PubMedCrossRefGoogle Scholar
  10. 10.
    Dashti M, Kulik W, Hoek F, Veerman EC, Peppelenbosch MP, Rezaee F (2011) A phospholipidomic analysis of all defined human plasma lipoproteins. Sci Rep 1:139PubMedCrossRefGoogle Scholar
  11. 11.
    Zhang W, Asztalos B, Roheim PS, Wong L (1998) Characterization of phospholipids in pre-alpha HDL: selective phospholipid efflux with apolipoprotein A-I. J Lipid Res 39:1601–1607PubMedGoogle Scholar
  12. 12.
    Piperi C, Kalofoutis C, Papaevaggeliou D, Papapanagiotou A, Lekakis J, Kalofoutis A (2004) The significance of serum HDL phospholipid levels in angiographically defined coronary artery disease. Clin Biochem 37:377–381PubMedCrossRefGoogle Scholar
  13. 13.
    Bovet P, Darioli R, Essinger A, Golay A, Sigwart U, Kappenberger L (1989) Phospholipids and other lipids in angiographically assessed coronary artery disease. Atherosclerosis 80:41–47PubMedCrossRefGoogle Scholar
  14. 14.
    Fournier N, de la Llera Moya M, Burkey BF, Swaney JB, Paterniti J Jr, Moatti N, Atger V, Rothblat GH (1996) Role of HDL phospholipid in efflux of cell cholesterol to whole serum: studies with human apoA-I transgenic rats. J Lipid Res 37:1704–1711PubMedGoogle Scholar
  15. 15.
    Mweva S, Paul JL, Cambillau M, Goudouneche D, Beaune P, Simon A, Fournier N (2006) Comparison of different cellular models measuring in vitro the whole human serum cholesterol efflux capacity. Eur J Clin Invest 36:552–559PubMedCrossRefGoogle Scholar
  16. 16.
    Klimov AN, Konstantinov VO, Lipovetsky BM, Kuznetsov AS, Lozovsky VT, Trufanov VF, Plavinsky SL, Gundermann KJ, Schumacher R (1995) “Essential” phospholipids versus nicotinic acid in the treatment of patients with type IIb hyperlipoproteinemia and ischemic heart disease. Cardiovasc Drugs Ther 9:779–784PubMedCrossRefGoogle Scholar
  17. 17.
    Bunea R, El Farrah K, Deutsch L (2004) Evaluation of the effects of Neptune Krill Oil on the clinical course of hyperlipidemia. Altern Med Rev 9:420–428PubMedGoogle Scholar
  18. 18.
    Mutungi G, Ratliff J, Puglisi M, Torres-Gonzalez M, Vaishnav U, Leite JO, Quann E, Volek JS, Fernandez ML (2008) Dietary cholesterol from eggs increases plasma HDL cholesterol in overweight men consuming a carbohydrate-restricted diet. J Nutr 138:272–276PubMedGoogle Scholar
  19. 19.
    Iwata T, Hoshi S, Takehisa F, Tsutsumi K, Furukawa Y, Kimura S (1992) The effect of dietary safflower phospholipid and soybean phospholipid on plasma and liver lipids in rats fed a hypercholesterolemic diet. J Nutr Sci Vitaminol (Tokyo) 38:471–479CrossRefGoogle Scholar
  20. 20.
    Wat E, Tandy S, Kapera E, Kamili A, Chung RW, Brown A, Rowney M, Cohn JS (2009) Dietary phospholipid-rich dairy milk extract reduces hepatomegaly, hepatic steatosis and hyperlipidemia in mice fed a high-fat diet. Atherosclerosis 205:144–150PubMedCrossRefGoogle Scholar
  21. 21.
    Kullenberg D, Taylor LA, Schneider M, Massing U (2012) Health effects of dietary phospholipids. Lipids Health Dis 11:3PubMedCrossRefGoogle Scholar
  22. 22.
    Zierenberg O, Grundy SM (1982) Intestinal absorption of polyenephosphatidylcholine in man. J Lipid Res 23:1136–1142PubMedGoogle Scholar
  23. 23.
    Weihrauch JL, Son Y-S (1983) The phospholipid content of foods. J Am Oil Chem Soc 60:1971–1978CrossRefGoogle Scholar
  24. 24.
    Cohn JS, Kamili A, Wat E, Chung RW, Tandy S (2010) Dietary phospholipids and intestinal cholesterol absorption. Nutrients 2:116–127PubMedCrossRefGoogle Scholar
  25. 25.
    Mutungi G, Waters D, Ratliff J, Puglisi M, Clark RM, Volek JS, Fernandez ML (2010) Eggs distinctly modulate plasma carotenoid and lipoprotein subclasses in adult men following a carbohydrate-restricted diet. J Nutr Biochem 21:261–267PubMedCrossRefGoogle Scholar
  26. 26.
    Blesso CN, Andersen CJ, Barona J, Volek JS, Fernandez ML (2013) Whole egg consumption improves lipoprotein profiles and insulin sensitivity to a greater extent than yolk-free egg substitute in individuals with metabolic syndrome. Metabolism 62:400–410PubMedCrossRefGoogle Scholar
  27. 27.
    Blesso CN, Andersen CJ, Bolling BW, Fernandez ML (2013) Egg intake improves carotenoid status by increasing plasma HDL cholesterol in adults with metabolic syndrome. Food Funct 31:213–221CrossRefGoogle Scholar
  28. 28.
    Hansel B, Giral P, Nobecourt E, Chantepie S, Bruckert E, Chapman MJ, Kontush A (2004) Metabolic syndrome is associated with elevated oxidative stress and dysfunctional dense high-density lipoprotein particles displaying impaired antioxidative activity. J Clin Endocrinol Metab 89:4963–4971PubMedCrossRefGoogle Scholar
  29. 29.
    (2001) Executive Summary of the third report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, And Treatment of High Blood Cholesterol In Adults (Adult Treatment Panel III). JAMA 285:2486–2497Google Scholar
  30. 30.
    Grundy SM, Brewer HB Jr, Cleeman JI, Smith SC Jr, Lenfant C (2004) Definition of metabolic syndrome: report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Arterioscler Thromb Vasc Biol 24:e13–e18PubMedCrossRefGoogle Scholar
  31. 31.
    Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18:499–502PubMedGoogle Scholar
  32. 32.
    Sorci-Thomas MG, Owen JS, Fulp B, Bhat S, Zhu X, Parks JS, Shah D, Jerome WG, Gerelus M, Zabalawi M, Thomas MJ (2012) Nascent high density lipoproteins formed by ABCA1 resemble lipid rafts and are structurally organized by three apoA-I monomers. J Lipid Res 53:1890–1909PubMedCrossRefGoogle Scholar
  33. 33.
    Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917PubMedCrossRefGoogle Scholar
  34. 34.
    Mayurasakorn K, Srisura W, Sitphahul P, Hongto PO (2008) High-density lipoprotein cholesterol changes after continuous egg consumption in healthy adults. J Med Assoc Thai 91:400–407PubMedGoogle Scholar
  35. 35.
    Klein BE, Klein R, Lee KE (2002) Components of the metabolic syndrome and risk of cardiovascular disease and diabetes in Beaver Dam. Diabetes Care 25:1790–1794PubMedCrossRefGoogle Scholar
  36. 36.
    Hong Y, Jin X, Mo J, Lin HM, Duan Y, Pu M, Wolbrette DL, Liao D (2007) Metabolic syndrome, its preeminent clusters, incident coronary heart disease and all—cause mortality-results of prospective analysis for the atherosclerosis risk in communities study. J Intern Med 262:113–122PubMedCrossRefGoogle Scholar
  37. 37.
    Shuhei N, Soderlund S, Jauhiainen M, Taskinen MR (2010) Effect of HDL composition and particle size on the resistance of HDL to the oxidation. Lipids Health Dis 9:104PubMedCrossRefGoogle Scholar
  38. 38.
    Park KH, Shin DG, Kim JR, Hong JH, Cho KH (2010) The functional and compositional properties of lipoproteins are altered in patients with metabolic syndrome with increased cholesteryl ester transfer protein activity. Int J Mol Med 25:129–136PubMedGoogle Scholar
  39. 39.
    Parra ES, Urban A, Panzoldo NB, Nakamura RT, Oliveira R, de Faria EC (2011) A reduction of CETP activity, not an increase, is associated with modestly impaired postprandial lipemia and increased HDL-cholesterol in adult asymptomatic women. Lipids Health Dis 10:87PubMedCrossRefGoogle Scholar
  40. 40.
    Lamarche B, Uffelman KD, Carpentier A, Cohn JS, Steiner G, Barrett PH, Lewis GF (1999) Triglyceride enrichment of HDL enhances in vivo metabolic clearance of HDL apo A-I in healthy men. J Clin Invest 103:1191–1199PubMedCrossRefGoogle Scholar
  41. 41.
    Skeggs JW, Morton RE (2002) LDL and HDL enriched in triglyceride promote abnormal cholesterol transport. J Lipid Res 43:1264–1274PubMedGoogle Scholar
  42. 42.
    Kinoshita M, Fujita M, Usui S, Maeda Y, Kudo M, Hirota D, Suda T, Taki M, Okazaki M, Teramoto T (2004) Scavenger receptor type BI potentiates reverse cholesterol transport system by removing cholesterol ester from HDL. Atherosclerosis 173:197–202PubMedCrossRefGoogle Scholar
  43. 43.
    Arsenault BJ, Lemieux I, Despres JP, Gagnon P, Wareham NJ, Stroes ES, Kastelein JJ, Khaw KT, Boekholdt SM (2009) HDL particle size and the risk of coronary heart disease in apparently healthy men and women: the EPIC-Norfolk prospective population study. Atherosclerosis 206:276–281PubMedCrossRefGoogle Scholar
  44. 44.
    Volek JS, Phinney SD, Forsythe CE, Quann EE, Wood RJ, Puglisi MJ, Kraemer WJ, Bibus DM, Fernandez ML, Feinman RD (2009) Carbohydrate restriction has a more favorable impact on the metabolic syndrome than a low fat diet. Lipids 44:297–309PubMedCrossRefGoogle Scholar
  45. 45.
    Smirnov MD, Esmon CT (1994) Phosphatidylethanolamine incorporation into vesicles selectively enhances factor Va inactivation by activated protein C. J Biol Chem 269:816–819PubMedGoogle Scholar
  46. 46.
    Griffin JH, Kojima K, Banka CL, Curtiss LK, Fernandez JA (1999) High-density lipoprotein enhancement of anticoagulant activities of plasma protein S and activated protein C. J Clin Invest 103:219–227PubMedCrossRefGoogle Scholar
  47. 47.
    Bradamante S, Barenghi L, Giudici GA, Vergani C (1992) Free radicals promote modifications in plasma high-density lipoprotein: nuclear magnetic resonance analysis. Free Radic Biol Med 12:193–203PubMedCrossRefGoogle Scholar
  48. 48.
    Navab M, Hama S, Hough G, Fogelman AM (2003) Oral synthetic phospholipid (DMPC) raises high-density lipoprotein cholesterol levels, improves high-density lipoprotein function, and markedly reduces atherosclerosis in apolipoprotein E-null mice. Circulation 108:1735–1739PubMedCrossRefGoogle Scholar
  49. 49.
    Wang H, Du J, Lu S, Yao Y, Hunter F, Black DD (2001) Regulation of intestinal apolipoprotein A-I synthesis by dietary phosphatidylcholine in newborn swine. Lipids 36:683–687PubMedCrossRefGoogle Scholar
  50. 50.
    Brunham LR, Kruit JK, Iqbal J, Fievet C, Timmins JM, Pape TD, Coburn BA, Bissada N, Staels B, Groen AK, Hussain MM, Parks JS, Kuipers F, Hayden MR (2006) Intestinal ABCA1 directly contributes to HDL biogenesis in vivo. J Clin Invest 116:1052–1062PubMedCrossRefGoogle Scholar
  51. 51.
    Rachmilewitz D, Fainaru M (1979) Apolipoprotein A-I synthesis and secretion by cultured human intestinal mucosa. Metabolism 28:739–743PubMedCrossRefGoogle Scholar
  52. 52.
    Xu M, Zhou H, Gu Q, Li C (2009) The expression of ATP-binding cassette transporters in hypertensive patients. Hypertens Res 32:455–461PubMedCrossRefGoogle Scholar
  53. 53.
    Xu M, Zhou H, Wang J, Li C, Yu Y (2009) The expression of ATP-binding cassette transporter A1 in Chinese overweight and obese patients. Int J Obes (Lond) 33:851–856CrossRefGoogle Scholar
  54. 54.
    Nakanishi S, Vikstedt R, Soderlund S, Lee-Rueckert M, Hiukka A, Ehnholm C, Muilu M, Metso J, Naukkarinen J, Palotie L, Kovanen PT, Jauhiainen M, Taskinen MR (2009) Serum, but not monocyte macrophage foam cells derived from low HDL-C subjects, displays reduced cholesterol efflux capacity. J Lipid Res 50:183–192PubMedCrossRefGoogle Scholar
  55. 55.
    Gantman A, Fuhrman B, Aviram M, Hayek T (2010) High glucose stimulates macrophage SR-BI expression and induces a switch in its activity from cholesterol efflux to cholesterol influx. Biochem Biophys Res Commun 391:523–528PubMedCrossRefGoogle Scholar
  56. 56.
    Wang X, Liao D, Bharadwaj U, Li M, Yao Q, Chen C (2008) C-reactive protein inhibits cholesterol efflux from human macrophage-derived foam cells. Arterioscler Thromb Vasc Biol 28:519–526PubMedCrossRefGoogle Scholar
  57. 57.
    Ervin RB (2009) Prevalence of metabolic syndrome among adults 20 years of age and over, by sex, age, race and ethnicity, and body mass index: United States, 2003–2006. Natl Health Stat Report:1–7Google Scholar
  58. 58.
    Dullaart RP, Groen AK, Dallinga-Thie GM, de Vries R, Sluiter WJ, van Tol A (2008) Fibroblast cholesterol efflux to plasma from metabolic syndrome subjects is not defective despite low high-density lipoprotein cholesterol. Eur J Endocrinol 158:53–60PubMedCrossRefGoogle Scholar
  59. 59.
    Alenezi MY, Marcil M, Blank D, Sherman M, Genest J Jr (2004) Is the decreased high-density lipoprotein cholesterol in the metabolic syndrome due to cellular lipid efflux defect? J Clin Endocrinol Metab 89:761–764PubMedCrossRefGoogle Scholar
  60. 60.
    Duong M, Collins HL, Jin W, Zanotti I, Favari E, Rothblat GH (2006) Relative contributions of ABCA1 and SR-BI to cholesterol efflux to serum from fibroblasts and macrophages. Arterioscler Thromb Vasc Biol 26:541–547PubMedCrossRefGoogle Scholar
  61. 61.
    Jian B, de la Llera-Moya M, Ji Y, Wang N, Phillips MC, Swaney JB, Tall AR, Rothblat GH (1998) Scavenger receptor class B type I as a mediator of cellular cholesterol efflux to lipoproteins and phospholipid acceptors. J Biol Chem 273:5599–5606PubMedCrossRefGoogle Scholar
  62. 62.
    Aron-Wisnewsky J, Julia Z, Poitou C, Bouillot JL, Basdevant A, Chapman MJ, Clement K, Guerin M (2011) Effect of bariatric surgery-induced weight loss on SR-BI-, ABCG1-, and ABCA1-mediated cellular cholesterol efflux in obese women. J Clin Endocrinol Metab 96:1151–1159PubMedCrossRefGoogle Scholar

Copyright information

© AOCS 2013

Authors and Affiliations

  • Catherine J. Andersen
    • 1
  • Christopher N. Blesso
    • 1
    • 3
  • Jiyoung Lee
    • 1
  • Jacqueline Barona
    • 1
    • 4
  • Dharika Shah
    • 2
  • Michael J. Thomas
    • 2
  • Maria Luz Fernandez
    • 1
  1. 1.Department of Nutritional SciencesUniversity of ConnecticutStorrsUSA
  2. 2.Biochemistry, Wake Forest School of MedicineWinston-SalemUSA
  3. 3.Pathology, Wake Forest School of MedicineWinston-SalemUSA
  4. 4.School of MicrobiologyUniversity of AntioquiaMedellinColombia

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