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Lipids

, Volume 45, Issue 12, pp 1127–1138 | Cite as

Postprandial Lipemia Detects the Effect of Soy Protein on Cardiovascular Disease Risk Compared with the Fasting Lipid Profile

  • Antonio S. SantoEmail author
  • Ariana M. Santo
  • Richard W. Browne
  • Harold Burton
  • John J. Leddy
  • Steven M. Horvath
  • Peter J. Horvath
Original Article

Abstract

Studies examining the effect of soy protein on cardiovascular disease (CVD) risk factors have not taken advantage of the postprandial state as an adjunct to the fasting lipid profile. The American Heart Association has acknowledged the efficacy of soy protein in reducing CVD risk factors to be limited. We hypothesized that the postprandial state would be more sensitive to any favorable changes associated with consuming soy protein compared with the fasting lipid profile. Furthermore, the presence of isoflavones in soy would enhance this effect. Thirty sedentary males aged 18–30 years were randomly assigned to milk protein (Milk), isoflavone-poor soy (Soy−), or isoflavone-rich soy (Soy+). Usual diets were supplemented with 25 g/day of protein for 28 days. Serum samples were collected before and after supplementation in a fasted state and postprandially at 30, 60, 120, 240, and 360 min after a high-fat, 1,000 kcal shake. Triacylglycerol (TAG), total cholesterol, non-esterified fatty acids, apolipoproteins B-100 and A-I and glucose concentrations were quantified. Fasting concentrations were not different after any protein supplementation. Postprandial TAG and TAG AUC increased after Soy-consumption supporting the postprandial state as a more sensitive indicator of soy ingestion effects on CVD risk factors compared with the fasting lipid profile. Furthermore, the absence of isoflavones in soy protein may have deleterious consequences on purported cardio-protective effects.

Keywords

Phytoestrogens Isoflavones Isoflavone-rich soy Soy protein Milk protein Postprandial metabolism Postprandial lipemia Hypertriacylglycerolemia Cardiovascular disease risk Triglycerides Lipid profile 

Abbreviations

CVD

Cardiovascular disease

Milk

Milk protein

Soy−

Isoflavone-poor soy

Soy+

Isoflavone-rich soy

TC

Total cholesterol

TAG

Triacylglycerol

Apo B-100

Apolipoprotein B-100

Apo A-I

Apolipoprotein A-I

FDA

Food and Drug Administration

VLDL

Very-low density lipoprotein

AUC

Area under the curve

BMI

Body mass index

HDL-C

High density lipoprotein cholesterol constituent

NEFA

Non-esterified fatty acids

ANOVA

Analysis of variance

LDL-C

Low density lipoprotein cholesterol constituent

RLP-C

Remnant-like particle-cholesterol

TRL

Triacylglycerol rich lipoprotein

LDL

Low density lipoprotein

HDL

High density lipoprotein

LCAT

Lecithin:cholesterol acyltransferase

Notes

Acknowledgments

The authors would like to thank The Solae Company (St. Louis, MO, USA) for donating the protein supplements used in this study. Special gratitude is warranted to our colleagues Amy Miracle and Jack Young for their input in the final review of this manuscript.

References

  1. 1.
    (2002) National Cholesterol Education Program (NCEP) Expert Panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III). 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) final report. Circulation 106:3143–3421Google Scholar
  2. 2.
    Adiels M, Packard C, Caslake MJ, Stewart P, Soro A, Westerbacka J, Wennberg B, Olofsson S-O, Taskinen M-R, Borén J (2005) A new combined multicompartmental model for apolipoprotein B-100 and triglyceride metabolism in VLDL subfractions. J Lipid Res 46:58–67CrossRefPubMedGoogle Scholar
  3. 3.
    Allen JK, Becker DM, Kwiterovich PO, Lindenstruth KA, Curtis C (2007) Effect of soy protein-containing isoflavones on lipoproteins in postmenopausal women. Menopause 14:106–114CrossRefPubMedGoogle Scholar
  4. 4.
    Anderson JW, O’Neal DS, Riddell-Mason S, Floore TM, Dillom DW, Oeltgen PR (1995) Postprandial serum glucose, insulin, and lipoprotein responses to high- and low-fiber diets. Metabolism 44:848–854CrossRefPubMedGoogle Scholar
  5. 5.
    Bansal S, Buring JE, Rifai N, Mora S, Sacks FM, Ridker PM (2007) Fasting compared with nonfasting triglycerides and risk of cardiovascular events in women. J Am Med Assoc 298:309–316CrossRefGoogle Scholar
  6. 6.
    Caldwell CR, Britz SJ, Mirecki RM (2005) Effect of temperature, elevated carbon dioxide, and draught during seed development on the isoflavone content of dwarf soybean [Glycine max (L.) Merrill] grown in controlled environments. J Agric Food Chem 53:1125–1129CrossRefPubMedGoogle Scholar
  7. 7.
    Cederroth CR, Nef S (2009) Soy, phytoestrogens and metabolism: a review. Mol Cell Endocrinol 304:30–42CrossRefPubMedGoogle Scholar
  8. 8.
    Cohn JS (2006) Postprandial lipemia and remnant lipoproteins. Clin Lab Med 26:773–786CrossRefPubMedGoogle Scholar
  9. 9.
    Cohn JS, McNamara JR, Cohn SD, Ordovas JM, Schaefer EJ (1988) Postprandial plasma lipoprotein changes in human subjects of different ages. J Lipid Res 29:469–479PubMedGoogle Scholar
  10. 10.
    Collaboration APCS (2004) Serum triglycerides as a risk factor for cardiovascular diseases in the Asia-Pacific Region. Circulation 110:2678–2686CrossRefGoogle Scholar
  11. 11.
    Coward L, Smith M, Kirk M, Barnes S (1998) Chemical modification of isoflavones in soy foods during cooking and processing. Am J Clin Nutr 68:1486s–1491sPubMedGoogle Scholar
  12. 12.
    De Bruin TWA, Brouwer B, Trip ML, Jansen H, Erkelens DW (1993) Different postprandial metabolism of olive oil and soybean oil: a possible mechanism of the high-density lipoprotein conserving effect of olive oil. Am J Clin Nutr 58:477–483PubMedGoogle Scholar
  13. 13.
    Dewell A, Hollenbeck PL, Hollenbeck CB (2006) Clinical review: a critical evaluation of the role of soy protein and isoflavone supplementation in the control of plasma cholesterol concentrations. J Clin Endocrinol Metab 91:772–780CrossRefPubMedGoogle Scholar
  14. 14.
    Freiberg JJ, Tybjaerg-Hansen A, Jensen JS, Nordestgaard BG (2008) Nonfasting triglycerides and risk of ischemic stroke in the general population. J Am Med Assoc 300:2142–2152CrossRefGoogle Scholar
  15. 15.
    Friedman M, Brandon DL (2001) Nutritional and health benefits of soy proteins. J Agric Food Chem 49:1069–1086CrossRefPubMedGoogle Scholar
  16. 16.
    Gardner CD, Messina M, Kiazand A, Morris JL, Franke AA (2007) Effect of two types of soy milk and dairy milk on plasma lipids in hypercholesterolemic adults: a randomized trial. J Am Coll Nutr 26:669–677PubMedGoogle Scholar
  17. 17.
    Ginsberg HN, Jones J, Blaner WS, Thomas A, Karmally W, Fields L, Blood D, Beg MD (1995) Association of postprandial triglyceride and retinyl palmitate responses with newly diagnosed exercise-induced myocardial ischemia in middle-aged men and women. Arterioscler Thromb Vasc Biol 15:1829–1838PubMedGoogle Scholar
  18. 18.
    Hanson LN, Engelman HM, Alekel DL, Schalinske KL, Kohut ML, Reddy MB (2006) Effects of soy isoflavones and phytate on homocysteine, C-reactive protein, and iron status in postmenopausal women. Am J Clin Nutr 84:774–780PubMedGoogle Scholar
  19. 19.
    Harris WS, Connor WE, Alam N, Illingworth DR (1988) Reduction of postprandial triglyceridemia in humans by dietary n-3 fatty acids. J Lipid Res 29:1451–1460PubMedGoogle Scholar
  20. 20.
    Ho SC, Chen YM, Ho SS, Woo JL (2007) Soy isoflavone supplementation and fasting serum glucose and lipid profile among postmenopausal Chinese women: a double-blind, randomized, placebo-controlled trial. Menopause 14:905–912CrossRefPubMedGoogle Scholar
  21. 21.
    Hooper L, Kroon PA, Rimm EB, Cohn JS, Harvey I, Le Cornu KA, Ryder JJ, Hall WL, Cassidy A (2008) Flavonoids, flavonoid-rich foods, and cardiovascular risk: a meta-analysis of randomized controlled trials. Am J Clin Nutr 88:38–50PubMedGoogle Scholar
  22. 22.
    Kannel WB, Vasan RS (2009) Triglycerides as vascular risk factors: new epidemiologic insights. Curr Opin Cardiol 24:345–350CrossRefPubMedGoogle Scholar
  23. 23.
    Karpe F, Steiner G, Uffelman K, Olivecrona T, Hamsten A (1994) Postprandial lipoprotein and progression of coronary atherosclerosis. Atherosclerosis 106:83–97CrossRefPubMedGoogle Scholar
  24. 24.
    Kolovou GD, Anagnostopoulou KK, Daskalopoulou SS, Mikhailidis DP, Cokkinos DV (2005) Clinical relevance of postprandial lipaemia. Curr Med Chem 12:1931–1945CrossRefPubMedGoogle Scholar
  25. 25.
    Langsted A, Freiberg JJ, Nordestgaard GB (2008) Fasting and nonfasting lipid levels: influence of normal food intake on lipids, lipoproteins, apolipoproteins, and cardiovascular risk prediction. Circulation 118:2047–2056CrossRefPubMedGoogle Scholar
  26. 26.
    Le N-A, Walter MF (2007) The role of hypertriglyceridemia in atherosclerosis. Curr Atheroscler Rep 9:110–115CrossRefPubMedGoogle Scholar
  27. 27.
    Levy E, Roy CC, Goldstein R, Bar-On H, Ziv E (1991) Metabolic fate of chylomicrons obtained from rats maintained on diets varying in fatty acid composition. J Am Coll Nutr 10:69–78PubMedGoogle Scholar
  28. 28.
    Lovati MR, Manzoni C, Corsini A, Granata A, Frattinin R, Fumagalli R, Sirtori CR (1992) Low density lipoprotein receptor activity is modulated by soybean globulins in cell culture. J Nutr 122:1971–1978PubMedGoogle Scholar
  29. 29.
    Lu LW, Anderson K (1998) Sex and long-term soy diets affect the metabolism and excretion of soy isoflavones in humans. Am J Clin Nutr 68:1500s–1504sPubMedGoogle Scholar
  30. 30.
    Ma Y, Chiriboga D, Olendzki BC, Nicolosi R, Merriam PA, Ockene IS (2005) Effect of soy protein containing isoflavones on blood lipids in moderately hypercholesterolemic adults: a randomized controlled trial. J Am Coll Nutr 24:275–285PubMedGoogle Scholar
  31. 31.
    Matthan NR, Jalbert SM, Ausman LM, Kuvin JT, Karas RH, Lichenstein AH (2007) Effect of soy protein from differently processed products on cardiovascular disease risk factors and vascular endothelial function in hypercholesterolemic subjects. Am J Clin Nutr 85:960–966PubMedGoogle Scholar
  32. 32.
    McVeigh BL, Dillingham BL, Lampe JW, Duncan AM (2006) Effect of soy protein varying in isoflavone content on serum lipids in healthy young men. Am J Clin Nutr 83:244–251PubMedGoogle Scholar
  33. 33.
    Mora S, Rifai N, Buring JE, Ridker PM (2008) Fasting compared with nonfasting lipids and apolipoproteins for predicting incident cardiovascular events. Circulation 118:993–1001CrossRefPubMedGoogle Scholar
  34. 34.
    Muesing RA, Griffin P, Mitchell P (1995) Corn oil and beef tallow elicit different postprandial responses in triglycerides and cholesterol, but similar changes in constituents of high-density lipoprotein. J Am Coll Nutr 14:53–60PubMedGoogle Scholar
  35. 35.
    Nordestgaard BG, Benn M, Schnohr P, Tybjaerg-Hansen A (2007) Nonfasting triglycerides and risk of myocardial infarction, ischemic heart disease, and death in men and women. J Am Med Assoc 298:299–308CrossRefGoogle Scholar
  36. 36.
    O’Keefe JH, Bell DSH (2007) Postprandial hyperglycemia/hyperlipidemia (postprandial dysmetabolism) is a cardiovascular risk factor. Am J Cardiol 100:899–904CrossRefPubMedGoogle Scholar
  37. 37.
    Otvos JD, Jeyarajah EJ, Cromwell WC (2002) Measurement issues related to lipoprotein heterogeneity. Am J Cardiol 90:22i–29iCrossRefPubMedGoogle Scholar
  38. 38.
    Parks EJ (2001) Recent findings in the study of postprandial lipemia. Curr Atheroscler Rep 3:462–470CrossRefPubMedGoogle Scholar
  39. 39.
    Patsch JR, Miesenbock G, Hopferwieser T, Muhlberger V, Knapp E, Dunn JK, Gotto AM, Patsch W (1992) Relation of triglyceride metabolism and coronary disease. Arterioscler Thromb 12:1336–1345PubMedGoogle Scholar
  40. 40.
    Pischon T, Girman CJ, Sacks FM, Rifai N, Stampfer MJ, Rimm EB (2005) Non-high-density lipoprotein cholesterol and apolipoprotein B in the prediction of coronary heart disease in men. Circulation 112:3375–3383CrossRefPubMedGoogle Scholar
  41. 41.
    Potter SM (1998) Soy protein and cardiovascular disease: the impact of bioactive components in soy. Nutr Rev 56:231–235CrossRefPubMedGoogle Scholar
  42. 42.
    Reynolds K, Chin A, Lees KA, Nguyen A, Bujnowski D, He J (2006) A meta-analysis of the effect of soy protein supplementation on serum lipids. Am J Cardiol 98:633–640CrossRefPubMedGoogle Scholar
  43. 43.
    Sacks FM (2006) The apolipoprotein story. Atheroscler Suppl 7:23–27CrossRefPubMedGoogle Scholar
  44. 44.
    Sacks FM, Lichenstein A, Horn LV, Harris W, Kris-Etherton P, Winston M (2006) Soy protein, isoflavones, and cardiovascular health: an American Heart Association Science Advisory for health professionals from the Nutrition Committee. Circulation 113:1034–1044CrossRefPubMedGoogle Scholar
  45. 45.
    Santo AS, Cunningham AM, Alhassan S, Browne RW, Burton H, Leddy JJ, Grandjean PW, Horvath SM, Horvath PJ (2008) NMR analysis of lipoprotein particle size does not increase sensitivity to the effect of soy protein on CVD risk when compared with the traditional lipid profile. Appl Physiol Nutr Metab 33:489–500CrossRefPubMedGoogle Scholar
  46. 46.
    Setchell K (1998) Phytoestrogens: the biochemistry, physiology, and implications for human health of soy isoflavones. Am J Clin Nutr 68:1333–1346Google Scholar
  47. 47.
    Sharret AR, Chambless LE, Heiss G, Paton CC, Patsch W (1995) Association of postprandial triglyceride and retinyl palmitate responses with asymptomatic carotid artery atherosclerosis in middle-aged men and women. Arterioscler Thromb Vasc Biol 15:2122–2129Google Scholar
  48. 48.
    Shige H, Ishikawa T, Higashi K, Yamashita T, Tomiyasu K, Yoshida H, Hosoai H, Ito T, Nakajima K, Ayaori M, Yonemura A, Suzukawa M, Nakamura H (1998) Effects of soy protein isolate (SPI) and casein on the postprandial lipemia in normolipidemic men. J Nutr Sci Vitaminol 44:113–127PubMedGoogle Scholar
  49. 49.
    Sirtori CR, Calabresi L, Franceschini G (1999) Recombinant apolipoproteins for the treatment of vascular diseases. Atherosclerosis 142:29–40CrossRefPubMedGoogle Scholar
  50. 50.
    Slavin JL, Karr SC, Hutchins AM, Lampe JW (1998) Influence of soybean processing, habitual diet, and soy dose on urinary isoflavonoid excretion. Am J Clin Nutr 68:1492s–1495sPubMedGoogle Scholar
  51. 51.
    Sniderman AD, Furberg CD, Keech A, JERv Lennep, Frohlich J, Jungner I, Walldius G (2003) Apolipoproteins versus lipids as indices of coronary risk and as targets for statin treatment. Lancet 361:777–780CrossRefPubMedGoogle Scholar
  52. 52.
    Stalenhoef AFH, Graaf Jd (2008) Association of fasting and nonfasting serum triglycerides with cardiovascular disease and the role of remnant-like lipoproteins and small dense LDL. Curr Opin Lipidol 19:355–361CrossRefPubMedGoogle Scholar
  53. 53.
    Taku K, Umegaki K, Sato Y, Endoh K, Watanabe S (2007) Soy isoflavones lower serum total and LDL cholesterol in humans: a meta-analysis of 11 randomized controlled trials. Am J Clin Nutr 85:1148–1156PubMedGoogle Scholar
  54. 54.
    Thorp A, Howe PRC, Mori TA, Coates AM, Buckley JD, Hodgson J, Mansour J, Meyer BJ (2008) Soy food consumption does not lower LDL cholesterol in either equol or nonequol producers. Am J Clin Nutr 88:298–304PubMedGoogle Scholar
  55. 55.
    Torres N, Torre-Villalvazo I, Tovar AR (2006) Regulation of lipid metabolism by soy protein and its implication in diseases mediated by lipid disorders. J Nutr Biochem 17:365–373CrossRefPubMedGoogle Scholar
  56. 56.
    Van Heek M, Zilversmit DB (1990) Postprandial lipemia and lipoprotein lipase in the rabbit are modified by olive and coconut oil. Arteriosclerosis 10:421–429PubMedGoogle Scholar
  57. 57.
    Wangen KE, Duncan AM, Xu X, Kurzer MS (2001) Soy isoflavones improve plasma lipids in normocholesterolemic and mildly hypercholesterolemic postmenopausal women. Am J Clin Nutr 73:225–231PubMedGoogle Scholar
  58. 58.
    Weintraub MS, Zechner R, Brown A, Eisenberg S, Breslow JL (1988) Dietary polyunsaturated fats of the w-6 and w-3 series reduce postprandial lipoproteins levels. J Clin Invest 82:1884–1893CrossRefPubMedGoogle Scholar
  59. 59.
    Weissberg PL, Rudd JH (eds) (2002) Atherosclerotic biology and epidemiology of disease textbook of cardiovascular medicine. Lippincott Williams & Wilkins, PhiladelphiaGoogle Scholar
  60. 60.
    Yu KC-W, Cooper AD (2001) Postprandial lipoproteins and atherosclerosis. Front Biosci 6:d332–d354CrossRefPubMedGoogle Scholar
  61. 61.
    Zhan S, Ho SC (2005) Meta-analysis of the effects of soy protein containing isoflavones on the lipid profile. Am J Clin Nutr 81:397–408PubMedGoogle Scholar
  62. 62.
    Zhuo X-G, Melby MK, Watanabe S (2004) Soy isoflavone intake lowers serum LDL cholesterol: a meta-analysis of 8 randomized controlled trials in humans. J Nutr 134:2395–2400PubMedGoogle Scholar
  63. 63.
    Zilversmit DB (1979) Atherogenesis: a postprandial phenomenon. Circulation 60:473–485PubMedGoogle Scholar

Copyright information

© AOCS 2010

Authors and Affiliations

  • Antonio S. Santo
    • 1
    • 2
    Email author
  • Ariana M. Santo
    • 3
  • Richard W. Browne
    • 4
  • Harold Burton
    • 5
  • John J. Leddy
    • 6
  • Steven M. Horvath
    • 7
  • Peter J. Horvath
    • 8
  1. 1.Department of Kinesiology and Nutrition SciencesUniversity of Nevada, Las Vegas School of Allied Health SciencesLas VegasUSA
  2. 2.Department of Exercise and Nutrition SciencesState University of New York at BuffaloBuffaloUSA
  3. 3.The Center for Diabetes Self-Management CareFrye Regional Medical CenterHickoryUSA
  4. 4.Biotechnical and Clinical Laboratory SciencesUniversity at Buffalo, State University of New YorkBuffaloUSA
  5. 5.Department of Exercise and Nutrition SciencesUniversity at Buffalo, State University of New YorkBuffaloUSA
  6. 6.Department of Exercise and Nutrition Sciences, Sports Medicine InstituteUniversity at Buffalo, State University of New YorkBuffaloUSA
  7. 7.Department of Exercise and Nutrition SciencesUniversity at Buffalo, State University of New YorkBuffaloUSA
  8. 8.Department of Exercise and Nutrition SciencesUniversity at Buffalo, State University of New YorkBuffaloUSA

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