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Reducing shell egg cholesterol content. II. Review of approaches utilizing non-nutritive dietary factors or pharmacological agents and an examination of emerging strategies

Published online by Cambridge University Press:  14 March 2007

R.G. ELKIN
R.G. ELKIN
Affiliation:
Department of Poultry Science, The Pennsylvania State University, University Park, PA 16802-3501USA
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Abstract

During the past four decades, research efforts directed toward reducing shell egg cholesterol content have centred on genetic selection or alteration of the laying hens' diet with various nutrients, natural products, non-nutritive factors, or pharmacological agents. However, the vast majority of these experimental approaches elicited only minimal changes (<10%) at best or, as in the case of dietary azasterols and triparanol, resulted in the unacceptable replacement of yolk cholesterol by desmosterol. In contrast, when 3-hydroxy-3-methylglutaryl-coenzyme A reductase inhibitors (‘statins’), garlic paste, or pharmacological amounts of copper were orally administered to chickens, yolk cholesterol levels were reduced by up to 46%, 32%, or 34%, respectively. The previous paper in this two-part series provided a justification for low-cholesterol egg production and reviewed cholesterol metabolism in the laying hen, avian embryonic cholesterol needs, and genetic and nutritional approaches to chicken egg cholesterol reduction. The present paper provides a comprehensive overview of the use of non-nutritive dietary factors and select pharmacological compounds as egg cholesterol-lowering agents, and discusses emerging strategies for lowering the cholesterol content of shell eggs. With the recent advances in avian genomics and transgenesis, it is anticipated that the greatest advances in the area of yolk cholesterol reduction will be attained through manipulation of key genes whose protein products mediate intestinal sterol absorption, hepatic cholesterol and lipoprotein synthesis, and/or lipoprotein uptake by growing oocytes. However, the future commercial availability of low-cholesterol eggs produced by transgenic hens ultimately will be influenced by the nature of the regulatory environment for bioengineered foods, public acceptance, and economics.

Keywords

cholesterolegg yolklaying henslipoproteinsvitellogeninVLDLstatinsavian transgenesis
Type
Review Article
Information
World's Poultry Science Journal , Volume 63 , Issue 1 , March 2007 , pp. 5 - 32
Copyright
Copyright © World's Poultry Science Association 2007

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References

ALBERTS, A.W. (1988) HMG-CoA reductase inhibitors – the development. Atherosclerosis Reviews 18: 123–131.Google Scholar
BARTOV, I., BORNSTEIN, S. and BUDOWSKI, P. (1971) Variability of cholesterol concentration in plasma and egg yolks of hens and evaluation of the effect of some dietary oils. Poultry Science 50: 1357–1364.Google Scholar
BAYS, H. and STEIN, E.A. (2003) Pharmacotherapy for dyslipidaemia – current therapies and future agents. Expert Opinion on Pharmacotherapeutics 4: 1901–1938.Google Scholar
BEYER, R.S. and JENSEN, L.S. (1990) Effect of high protein barley flour and cholesterol on tissue and egg cholesterol of SCWL laying hens. Poultry Science 69 (suppl. 1): 18. (Abstr.).Google Scholar
BEYER, R.S. and JENSEN, L.S. (1991) Influence of orotic acid on performance, liver lipid content, and egg cholesterol level of laying hens. Poultry Science 70: 2322–2328.CrossRefGoogle ScholarPubMed
BEYER, R.S. and JENSEN, L.S. (1992) Cholesterol concentration of egg yolk and blood plasma and performance of laying hens as influenced by dietary α-ketoisocaproic acid. Poultry Science 71: 120–127.Google Scholar
BEYER, R.S. and JENSEN, L.S. (1993a) Reduced plasma cholesterol and lipoprotein in laying hens without concomitant reduction of egg cholesterol in response to dietary sorbose. Poultry Science 72: 88–97.Google Scholar
BEYER, R.S. and JENSEN, L.S. (1993b) The hypocholesterolemic agent dichloroacetate increases egg cholesterol content of laying hens. Poultry Science 72: 1063–1069.Google Scholar
BJÖRKHEM, I. and DICZFALUSY, U. (2002) Oxysterols: Friends, foes, or just fellow passengers? Arteriosclerosis, Thrombosis, and Vascular Biology 22: 734–742.Google Scholar
BOCAN, T.M.A., MUELLER, S.B., UHLENDORF, P.D., NEWTON, R.S. and KRAUSE, B.R. (1991) Comparison of CI-976, and ACAT inhibitor, and selected lipid-lowering agents for antiatherosclerotic activity in iliac-femoral and thoracic aortic lesions. A biochemical, morphological, and morphometric evaluation. Arteriosclerosis and Thrombosis 11: 1830–1843.CrossRefGoogle ScholarPubMed
BRAUN, A., ZHANG, S., MIETTINEN, H.E., EBRAHIM, S., HOLM, T.M., VASILE, E., POST, M.J., YOERGER, D.M., PICARD, M.H., KRIEGER, J.L., ANDREWS, N.C., SIMONS, M. and KRIEGER, M. (2003) Probucol prevents early coronary heart disease and death in the high-density lipoprotein receptor SR-BI/apolipoprotein E double knockout mouse. Proceedings of the National Academy of Sciences USA 100: 7283–7288.Google Scholar
BROWN, L., ROSNER, B., WILLETT, W.W. and SACKS, F.M. (1999) Cholesterol-lowering effects of dietary fiber: A meta-analysis. American Journal of Clinical Nutrition 69: 30–42.CrossRefGoogle ScholarPubMed
BRUCKERT, E., GIRAL, P. and TELLIER, P. (2003) Perspectives in cholesterol-lowering therapy. The role of ezetimibe, a new selective inhibitor of intestinal cholesterol absorption. Circulation 107: 3124–3128.CrossRefGoogle ScholarPubMed
BURGESS, T.L., BURGESS, C.L. and WILSON, J.D. (1962) Effect of MER-29 on egg production in the chicken. Proceedings of the Society for Experimental Biology and Medicine 109: 218–221.CrossRefGoogle ScholarPubMed
BURT, D. and POURQUIE, O. (2003) Chicken genome – science nuggets to come soon. Science 300: 1669.Google Scholar
CECIL, H.C., BITMAN, J., SVOBODA, J.A. and THOMPSON, M.J. (1981) Effects of branched and straight chain amines and azasteroids on blood and egg cholesterol of White Leghorn chickens. Poultry Science 60: 795–804.CrossRefGoogle ScholarPubMed
CHOWDHURY, S.R., CHOWDHURY, S.D. and SMITH, T.K. (2002) Effects of dietary garlic on cholesterol metabolism in laying hens. Poultry Science 81: 1856–1862.CrossRefGoogle ScholarPubMed
CLARENBURG, R., CHUNG, I.A.K. and WAKEFIELD, L.M. (1971) Reducing the egg cholesterol level by including emulsified sitosterol in standard chicken diet. Journal of Nutrition 101: 289–298.CrossRefGoogle ScholarPubMed
CLARK, J. and WHITELAW, B. (2003) A future for transgenic livestock. Nature Reviews. Genetics 4: 825–833.CrossRefGoogle ScholarPubMed
Council On Scientific Affairs (1989) Dietary fiber and health. JAMA: The Journal of the American Medical Association 262: 542–546.CrossRefGoogle Scholar
CUNNINGHAM, D.L., KRUEGER, W.F., FANGUY, R.C. and BRADLEY, J.W. (1974) Preliminary results of bidirectional selection for yolk cholesterol level in laying hens. Poultry Science 53: 384–391.CrossRefGoogle ScholarPubMed
DAM, H. (1928) Die synthese und resorption des cholesterins beleuchtet durch versuche an huhnereiern. Biochemische Zeitschrift 194: 188–196.Google Scholar
DAM, H. (1929) Cholesterinstoffwechsel in huhnereiern und huhnchen. Biochemische Zeitschrift 215: 475–492.Google Scholar
DAM, R., LABATE, M.E., TAM, S.W. and CUERVO-TORRES, C. (1979) Effects of diazacholesterol, triparanol, and β-sitosterol on egg cholesterol deposition in Coturnix quail. Poultry Science 58: 985–987.Google Scholar
DE JONG, A., PLAT, J. and MENSINK, R.P. (2003) Metabolic effects of plant sterols and stanols. Journal of Nutritional Biochemistry 14: 362–369.Google Scholar
DE SCHIJVER, R. (1995) Lipid composition of egg yolk and blood plasma as influenced by dietary clenbuterol and cholesterol. INFORM 6(4): 472.Google Scholar
ELKIN, R.G. (2006) Reducing shell egg cholesterol content. I. Overview, genetic approaches, and nutritional strategies. World's Poultry Science Journal 62: 665–687.Google Scholar
ELKIN, R.G., FREED, M.B., KIEFT, K.A. and NEWTON, R.S. (1993a) Alteration of egg yolk cholesterol content and plasma lipoprotein profiles following administration of a totally synthetic HMG-CoA reductase inhibitor to laying hens. Journal of Agricultural and Food Chemistry 41: 1094–1101.CrossRefGoogle Scholar
ELKIN, R.G., FREED, M., WATKINS, B.A., SREBNIK, M., KIEFT, K.A. and NEWTON, R.S. (1993b) Evaluation of two novel biochemicals on plasma and egg yolk lipid composition and laying hen performance. Poultry Science 72: 513–520.CrossRefGoogle ScholarPubMed
ELKIN, R.G., FURUMOTO, E.J. and THOMAS, C.R. (2003a) Assessment of egg nutrient compositional changes and residue in eggs, tissues, and excreta following oral administration of atorvastatin to laying hens. Journal of Agricultural and Food Chemistry 51: 3473–3481.CrossRefGoogle ScholarPubMed
ELKIN, R.G. and LORENZ, E.S. (2003) The egg is refractory to soy sterol enrichment through alteration of the hen's diet. Poultry Science 82 (suppl. 1): 52. (Abstr.).Google Scholar
ELKIN, R.G. and ROGLER, J.C. (1990) Reduction of the cholesterol content of eggs by the oral administration of lovastatin to laying hens. Journal of Agricultural and Food Chemistry 38: 1635–1641.Google Scholar
ELKIN, R.G., ROGLER, J.C., LEE, H.D. and WATKINS, B.A. (1992) Effect of β, β’-tetramethylsubstituted hexadecanedioic acid (MEDICA 16) on laying hen performance and egg yolk lipid composition. British Poultry Science 33: 677–681.Google Scholar
ELKIN, R.G., YAN, Z., ZHONG, Y., DONKIN, S.S., BUHMAN, K.K., STORY, J.A., TUREK, J.J., PORTER, R.E., ANDERSON, M., HOMAN, R. and NEWTON, R.S. (1999) Select 3-hydroxy-3-methylglutaryl-coenzyme A reductase inhibitors vary in their ability to reduce egg yolk cholesterol levels in laying hens through alteration of hepatic cholesterol biosynthesis and plasma VLDL composition. Journal of Nutrition 129: 1010–1019.Google Scholar
ELKIN, R.G., ZHONG, Y., DONKIN, S.S., HENGSTSCHLÄGER-OTTNAD, E. and SCHNEIDER, W.J. (2006) Effects of atorvastatin on lipid metabolism in normolipidemic and hereditary hyperlipidemic, nonlaying hens. Comparative Biochemistry and Physiology, Part B: 143: 319–329.CrossRefGoogle Scholar
ENDO, A. (1980) Biological and biochemical aspects of ML-236B (compactin) and monacolin K, specific competitive inhibitors of 3-hydroxy-3-methylglutaryl coenzyme A reductase. Pages 152–155. in Atherosclerosis V, Proceedings of the Fifth International Symposium. Gotto, A.M., Smith, L.C. and Allen, B. (ed.) Springer-Verlag, New York.Google Scholar
ENDO, A. (1992) The discovery and development of HMG-CoA reductase inhibitors. Journal of Lipid Research 33: 1569–1582.Google Scholar
ENDO, A., KITANO, N. and FUJII, S. (1978) Effects of ML-236B, a competitive inhibitor of 3-hydroxy-3-methylglutaryl (HMG)-CoA reductase, on cholesterol metabolism. Advances in Experimental Medicine and Biology 109: 376.Google Scholar
FRANCIS, G., KAREN, Z., MAKKAR, H.P.S. and BECKER, K. (2002) The biological action of saponins in animal systems: A review. British Journal of Nutrition 88: 587–605.Google Scholar
GAO, B., SUN, H.C., FANG, H.X., QIAN, K., ZHAO, M.S., QIU, H.L., SONG, C.Y. and WANG, Z.Y. (2006) Expression and preliminary characterization of recombinant human tissue kallikrein in egg white of laying hens. Poultry Science 85: 1239–1244.CrossRefGoogle ScholarPubMed
GIBBONS, G.F., WIGGINS, D., BROWN, A.-M. and HEBBACHI, A.-M. (2004) Synthesis and function of hepatic very-low density lipoprotein. Biochemical Society Transactions 32 (Part 1): 59–64.CrossRefGoogle ScholarPubMed
GOLDSTEIN, J.L. and BROWN, M.S. (1990) Regulation of the mevalonate pathway. Nature 343: 425–430.CrossRefGoogle ScholarPubMed
GRIFFIN, H.D. (1992) Manipulation of egg yolk cholesterol: A physiologist's view. World's Poultry Science Journal 48: 101–112.CrossRefGoogle Scholar
HARGIS, P.S. (1988) Modifying egg yolk cholesterol in the domestic fowl: a review. World's Poultry Science Journal 44: 17–29.CrossRefGoogle Scholar
HARRIS, P.C. and WILCOX, F.H. (1963) Studies on egg yolk cholesterol. 3. Effect of dietary cholesterol. Poultry Science 42: 186–189.CrossRefGoogle Scholar
HARVEY, A.J. and IVARIE, R. (2003) Validating the hen as a bioreactor for the production of exogenous proteins in egg white. Poultry Science 82: 927–930.CrossRefGoogle ScholarPubMed
HARVEY, A.J., SPEKSNIJDER, G., BAUGH, L.R., MORRIS, J.A. and IVARIE, R. (2002) Expression of exogenous protein in the egg white of transgenic chickens. Nature Biotechnology 19: 396–399.Google Scholar
HEBER, D., YIP, I., ASHLEY, J.M., ELASHOFF, D.A., ELASHOFF, R.M. and GO, V.L.W. (1999) Cholesterol-lowering effects of a proprietary Chinese red-yeast-rice dietary supplement. American Journal of Clinical Nutrition 69: 231–236.CrossRefGoogle ScholarPubMed
HEBERT, J.A. and ACHEE, V.N. (1993) Comparison of fibrate drugs on cholesterol in laying hens. FASEB Journal 7: A567. (Abstr.).Google Scholar
HIYOSHI, H., YANAGIMACHI, M., ITO, M., YASUDA, N., OKADA, T., IKUTA, H., SHINMYO, D., TANAKA, K., KURUSU, N., YOSHIDA, I., ABE, S., SAEKI, T. and TANAKA, H. (2003) Squalene synthase inhibitors suppress triglyceride biosynthesis through the farnesol pathway in rat hepatocytes. Journal of Lipid Research 44: 128–135.CrossRefGoogle ScholarPubMed
HOLMES, W.L. and BENTZ, J.D. (1960) Inhibition of cholesterol biosynthesis in vitro by β-diethylaminoethyl diphenylpropylacetate hydrocholoride (SKF 525-A). Journal of Biological Chemistry 235: 3118–3122.CrossRefGoogle Scholar
HOOD, R.L., BAILEY, W.MCC. and SVORONOS, D. (1978) The effect of dietary monoterpenes on the cholesterol level of eggs. Poultry Science 57: 304–306.CrossRefGoogle ScholarPubMed
HUGGETT, C.D., BUTTERY, P.J. and SALTER, A.M. (1993) Plasma VLDL cholesterol and egg cholesterol are resistant to change in the laying hen. Biochemical Society Transactions 21: 147S.CrossRefGoogle ScholarPubMed
HUNNINGHAKE, D.B. (1988) Clinical trials of lovastatin and simvastatin versus cholestyramine. Atherosclerosis Reviews 18: 133–138.Google Scholar
INTERNATIONAL CHICKEN GENOME SEQUENCING CONSORTIUM (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432: 695–716.CrossRefGoogle Scholar
IVARIE, R. (2003) Avian transgenesis: Progress towards the promise. Trends in Biotechnology 21: 14–19.CrossRefGoogle ScholarPubMed
IZZAT, N.N., DESHAZER, M.E. and LOOSE-MITCHELL, D.S. (2000) New molecular targets for cholesterol-lowering therapy. Journal of Pharmacology and Experimental Therapeutics 293: 315–320.Google ScholarPubMed
JIANG, Z. and SIM, J.S. (1991) Egg cholesterol values in relation to the age of laying hens and to egg and yolk weights. Poultry Science 70: 1838–1841.CrossRefGoogle Scholar
JONES, D. (1969) Variations in the cholesterol content of egg yolk. Nature 221: 780.CrossRefGoogle ScholarPubMed
KAJINAMI, K., MABUCHI, H. and SAITO, Y. (2000) NK-104: A novel synthetic HMG-CoA reductase inhibitor. Expert Opinion on Investigational Drugs 9: 2653–2661.CrossRefGoogle ScholarPubMed
KAJINAMI, K., TAKEKOSHI, N. and SAITO, Y. (2003) Pitavastatin: Efficacy and safety profiles of a novel synthetic HMG-CoA reductase inhibitor. Cardiovascular Drug Reviews 21: 199–215.CrossRefGoogle ScholarPubMed
KANDUTSCH, A.A., CHEN, H.W. and HEINIGER, H.-J. (1978) Biological activity of some oxygenated sterols. Science 201: 498–501.CrossRefGoogle ScholarPubMed
KAYA, S., ERDOGAN, Z. and ERDOGAN, S. (2003) Effect of different dietary levels of Yucca schidigera powder on the performance, blood parameters, and egg yolk cholesterol of laying quails. Journal of Veterinary Medicine. A, Physiology, Pathology, Clinical Medicine 50: 14–17.CrossRefGoogle ScholarPubMed
KIM, J.H., HONG, S.T., LEE, H.S. and KIM, H.J. (2004) Oral administration of pravastatin reduces egg cholesterol but not plasma cholesterol in laying hens. Poultry Science 83: 1539–1543.Google Scholar
KIM, S., CHAO, P.Y. and ALLEN, K.G. (1992) Inhibition of elevated hepatic glutathione abolishes copper deficiency cholesterolemia. FASEB Journal 6: 2467–2471.CrossRefGoogle ScholarPubMed
KONLANDE, J.E. and FISHER, H. (1969) Evidence for a nonabsorptive antihypercholesterolemic action of phytosterols in the chicken. Journal of Nutrition 98: 435–442.CrossRefGoogle ScholarPubMed
KRAUSE, B.R., BLACK, A., BOUSLEY, R., ESSENBURG, A., CORNICELLI, J., HOLMES, A., HOMAN, R., KIEFT, K., SEKERKE, C. and SHAW-HES, M.K. (1993) Divergent pharmacologic activities of PD 132301-2 and CL 277,082, urea inhibitors of acyl-CoA:cholesterol acyltransferase. Journal of Pharmacology and Experimental Therapeutics 267: 734–743.Google ScholarPubMed
KUDCHODKAR, B.J., HORLICK, L. and O'NEILL, J.B. (1976) Absorption of dietary β-sitosterol in laying hens and its incorporation into the egg. Journal of Nutrition 106: 1629–1636.CrossRefGoogle ScholarPubMed
LILLICO, S.G., McGREW, M.J., SHERMAN, A. and SANG, H.M. (2005) Transgenic chickens as bioreactors for protein-based drugs. Drug Discovery Today 10: 191–196.CrossRefGoogle ScholarPubMed
LIRETTE, A., ROBINSON, A.R., CROBER, D.C., LAWSON, P.D. and FIRTH, N.L. (1993) Effect of oat bran, cotton seed hulls and guar gum on chicken egg and blood lipids during the early laying period. Canadian Journal of Animal Science 73: 673–677.CrossRefGoogle Scholar
LUHMAN, C.M., MILLER, B.G. and BEITZ, D.C. (1990) The effect of feeding lovastatin and colestipol on production and cholesterol content of eggs. Poultry Science 69: 852–855.CrossRefGoogle ScholarPubMed
MAGNIN, D.R., BILLER, S.A., WETTERAU, J., ROBL, J.A., DICKSON, J.K., TAUNK, P., HARRITY, T.W., LAWRENCE, R.M., SUN, C.-Q., WANG, T., LOGAN, J., FRYSZMAN, O., CONNOLLY, F., JOLIBOIS, K. and KUNSELMAN, L. (2003) Microsomal triglyceride transfer protein inhibitors: Discovery and synthesis of alkyl phosphonates as potent MTP inhibitors and cholesterol lowering agents. Bioorganic & Medicinal Chemistry Letters 13: 1337–1340.CrossRefGoogle ScholarPubMed
MAYES, P.A. (1996) Cholesterol synthesis, transport, and excretion. Pages 271–283. in Harper's Biochemistry, 24th edition. Murray, R.K., Granner, D.K., Mayes, P.A. and Rodwell, V.W. (ed.). Appleton & Lange, Stamford, CT.Google Scholar
McGINNIS, C.H. and RINGER, R.K. (1963) The effect of a quaternary ammonium anion exchange resin on plasma and egg yolk cholesterol in the laying hen. Poultry Science 42: 394–396.CrossRefGoogle Scholar
McGONIGLE, K.E.M. and McCRACKEN, K.J. (2002.) Study on the effects of Annatto (Bixa orellana) and Yucca shidegera on cholesterol content and yolk colour. British Poultry Science 43: S41–S42.Google Scholar
McNAMARA, D.J., KOLB, R., PARKER, T.S., BATWIN, H., SAMUEL, P., BROWN, C.D. and AHRENS, E.H. (1987) Heterogeneity of cholesterol homeostasis in man. Response to changes in dietary fat quality and cholesterol quantity. Journal of Clinical Investigation 79: 1729–1739.Google Scholar
McNAUGHTON, J.L. (1978) Effect of dietary fiber on egg yolk, liver, and plasma cholesterol concentrations of the laying hen. Journal of Nutrition 108: 1842–1848.Google Scholar
MENGE, H., LITTLEFIELD, L.H., FROBISH, L.T. and WEINLAND, B.T. (1974) Effect of cellulose and cholesterol on blood and yolk lipids and reproductive efficiency of the hen. Journal of Nutrition 104: 1554–1566.CrossRefGoogle ScholarPubMed
MERSMANN, H.J. (1998) Overview of the effects of β-adrenergic receptor agonists on animal growth including mechanisms of action. Journal of Animal Science 76: 160–172.CrossRefGoogle ScholarPubMed
MICHIHARA, A., SAWAMURA, M., YAMORI, Y., AKASAKI, K. and TSUJI, H. (2003) Probucol decreases mevalonate pyrophosphate decarboxylase in the rat liver. Biological & Pharmaceutical Bulletin 26: 1484–1486.Google Scholar
MIYAZAKI, A., SAKAI, M., SAKAMOTO, Y. and HORIUCHI, S. (2003) Acyl-coenzyme A:cholesterol acyltransferase inhibitors for controlling hypercholesterolemia and atherosclerosis. Current Opinion in Investigational Drugs 4: 1095–1099.Google ScholarPubMed
MOREAU, R.A., WHITAKER, B.D. and HICKS, K.B. (2002) Phytosterols, phytostanols, and their conjugates in foods: Structural diversity, quantitative analysis, and health-promoting uses. Progress in Lipid Research 41: 457–500.CrossRefGoogle ScholarPubMed
MORI, A.V., MENDONCA, C.X. and SANTOS, C.O.F. (1999) Effect of dietary lipid-lowering drugs upon plasma lipids and egg yolk cholesterol levels of laying hens. Journal of Agricultural and Food Chemistry 47: 4731–4735.Google Scholar
NABER, E.C. (1976) The cholesterol problem, the egg and lipid metabolism in the laying hen. Poultry Science 55: 14–30.CrossRefGoogle ScholarPubMed
NABER, E.C. (1983) Nutrient and drug effects on cholesterol metabolism in the laying hen. Federation Proceedings 42: 2486–2493.Google ScholarPubMed
NABER, E.C. (1990) Cholesterol content of eggs: Can and should it be changed? Feedstuffs 62(5): 1, 47, 50–52.Google Scholar
NABER, E.C., ALLRED, J.B., WINGET, C.J. and STOCK, A.E. (1985) Effect of cholesterol oxidation products on cholesterol metabolism in the laying hen. Poultry Science 64: 675–680.CrossRefGoogle ScholarPubMed
NABER, E.C., ELLIOTT, J.F. and SMITH, T.L. (1982) Effect of probucol on reproductive performance, egg yolk cholesterol content, and lipid metabolism in the laying hen. Poultry Science 61: 1118–1124.Google Scholar
NAKAUE, H.S., LOWRY, R.R., CHEEKE, P.R. and ARSCOTT, G.H. (1980) The effect of dietary alfalfa of varying saponin content on yolk cholesterol level and layer performance. Poultry Science 59:2744–2748.Google Scholar
NATIONAL RESEARCH COUNCIL (1984) Nutrient Requirements of Poultry, 8th revised edition. National Academy Press, Washington, DC.Google Scholar
NELSON, S.J., CLEGG, R.E. and SANFORD, P.E. (1962) The effect of triparanol on calcium and cholesterol levels in the blood sera of laying hens. Poultry Science 41: 664–668.CrossRefGoogle Scholar
NICHOLS, E.L. and BALLOUN, S.L. (1962) Effects of the hypocholesteremic agent SC-11952 on the laying hen. Poultry Science 41: 1982–1984.CrossRefGoogle Scholar
NICHOLS, E.L., MARION, W.W. and BALLOUN, S.L. (1962) Influence of triparanol (MER29) on growth, egg production, and cholesterol metabolism of chickens. Poultry Science 41: 1494–1499.CrossRefGoogle Scholar
NICHOLS, E.L., MARION, W.W. and BALLOUN, S.L. (1963) Effect of egg yolk size on yolk cholesterol concentration. Proceedings of the Society for Experimental Biology and Medicine 112: 378–380.CrossRefGoogle ScholarPubMed
NISHIOKA, T., HYOGO, H., NUMATA, Y., YAMAGUCHI, A., KOBUKE, T., KOMICHI, D., NONAKA, M., INOUE, M., NABESHIMA, Y., OGI, M., IWAMOTO, K., ISHITOBI, T., AJIMA, T., CHAYAMA, K. and TAZUMA, S. (2005) A nuclear receptor-mediated choleretic action of fibrates is associated with enhanced canalicular membrane fluidity and transporter activity mediating bile acid-independent bile secretion. Journal of Atherosclerosis and Thrombosis 12: 211–217.CrossRefGoogle ScholarPubMed
OSTLUND, R.E. (2002) Phytosterols in human nutrition. Annual Review of Nutrition 22: 533–549.Google Scholar
OSTLUND, R.E. (2004) Phytosterols and cholesterol metabolism. Current Opinion in Lipidology 15: 37–41.CrossRefGoogle ScholarPubMed
OSTLUND, R.E., SPILBURG, C.A. and STENSON, W.F. (1999) Sitostanol administered in lecithin micelles potently reduces cholesterol absorption in humans. American Journal of Clinical Nutrition 70: 826–831.CrossRefGoogle ScholarPubMed
PESTI, G.M. and BAKALLI, R.I. (1998) Studies on the effect of feeding cupric sulfate pentahydrate to laying hens on egg cholesterol content. Poultry Science 77: 1540–1545.CrossRefGoogle ScholarPubMed
PETERSON, D.W. (1951) Effect of soybean sterols in the diet on plasma and liver cholesterol in chicks. Proceedings of the Society for Experimental Biology and Medicine 78: 143–147.CrossRefGoogle ScholarPubMed
POLLAK, O.J. (1953) Reduction of blood cholesterol in man. Circulation 7: 702–706.Google Scholar
QURESHI, A.A., PETERSON, D.M., DIN, Z.Z., ELSON, C.E. and BITGOOD, J.J. (1986) The independent roles of genetic and dietary factors in determining the cholesterol status of laying hens. Nutrition Reports International 34: 457–464.Google Scholar
QURESHI, A.A., PRENTICE, N., DIN, Z.Z., BURGER, W.C., ELSON, C.E. and SUNDE, M.L. (1984) Influence of culture filtrate of Trichoderma viride and barley on lipid metabolism of laying hens. Lipids 19: 250–257.Google Scholar
RAAL, F.J., MARAIS, A.D., KLEPACK, E., LOVALVO, J., MCLAIN, R. and HEINONEN, T. (2003) Avasimibe, an ACAT inhibitor, enhances the lipid lowering effect of atorvastatin in subjects with homozygous familial hypercholesterolemia. Atherosclerosis 171: 273–279.CrossRefGoogle ScholarPubMed
ROTENBERG, S. and MASON, V.C. (1977) The influence of dietary pectin on the cholesterol content of egg yolk and muscle and on various haematological indices in laying hens. Nordisk Veterinaermedicin 29: 30–35.Google ScholarPubMed
RYBAK, M.E., CALVEY, E.M. and HARNLY, J.M. (2004) Quantitative determination of allicin in garlic: Supercritical fluid extraction and standard addition of alliin. Journal of Agricultural and Food Chemistry 52: 682–687.CrossRefGoogle ScholarPubMed
SANG, H. (2004) Prospects for transgenesis in the chick. Mechanisms of Development 121: 1179–1186.Google Scholar
SHAFEY, T.M., DINGLE, J.G. and MCDONALD, M.W. (1992) Comparison between wheat, triticale, rye, soyabean oil and strain of laying bird on the production, and cholesterol and fatty acid contents of eggs. British Poultry Science 33: 339–346.Google Scholar
SHAH, P.K. (2003) Emerging non-statin LDL-lowering therapies for dyslipidemia and atherosclerosis. Reviews in Cardiovascular Medicine 4: 136–141.Google ScholarPubMed
SHAKLEE, W.E. (1972) Research on cholesterol in poultry and eggs in the United States. World's Poultry Science Journal 28: 389–399.Google Scholar
SHELNESS, G.S. and SELLERS, J.A. (2001) Very-low-density lipoprotein assembly and secretion. Current Opinion in Lipidology 12: 151–157.CrossRefGoogle ScholarPubMed
SHUMAN, R.M. (1991) Production of transgenic birds. Experientia 47: 897–905.Google Scholar
SIM, J.S. and BRAGG, D.B. (1977) Effect of dietary factors on serum and egg yolk cholesterol levels of laying hens. Poultry Science 56: 1616–1621.CrossRefGoogle ScholarPubMed
SIM, J.S., KITTS, W.D. and BRAGG, D.B. (1984) Effect of dietary saponin on egg cholesterol level and laying hen performance. Canadian Journal of Animal Science 64: 977–984.CrossRefGoogle Scholar
SINGH, R.A. (1972) Effect of D-thyroxine and nicotinic acid on cholesterol metabolism of laying hens. Indian Journal of Animal Science 42: 433–435.Google Scholar
STAELS, B., DALLONGEVILLE, J., AUWERX, J., SCHOONJANS, K., LEITERSDORF, E. and FRUCHART, J.-C. (1998) Mechanism of action of fibrates on lipid and lipoprotein metabolism. Circulation 98: 2088–2093.Google Scholar
STEINBERG, D. (2006) An interpretive history of the cholesterol controversy, part V: The discovery of the statins and the end of the controversy. Journal of Lipid Research 47: 1339–1351.Google Scholar
STIFANI, S., NIMPF, J. and SCHNEIDER, W.J. (1990) Vitellogenesis in Xenopus laevis and chicken: Cognate ligands and oocyte receptors. Journal of Biological Chemistry 265: 882–888.CrossRefGoogle ScholarPubMed
TENNENT, D.M., SIEGEL, H., ZANETTI, M.E., KURON, G.W., OTT, W.H. and WOLF, F.J. (1960) Plasma cholesterol lowering action of bile acid binding polymers in experimental animals. Journal of Lipid Research 1: 469–473.CrossRefGoogle ScholarPubMed
TOBERT, J.A. (2003) Lovastatin and beyond: The history of the HMG-CoA reductase inhibitors. Nature Reviews. Drug Discovery 2: 517–526.Google Scholar
TURK, D.E. and BARNETT, B.D. (1972) Diet and egg cholesterol content. Poultry Science 51: 1881. (Abstr.).Google Scholar
TURNER, S.W., JUNGBLUTH, G.L. and KNUTH, D.W. (2002) Effect of concomitant colestipol hydrochloride administration on the bioavailability of diltiazem from immediate- and sustained-release formulations. Biopharmaceutics & Drug Disposition 23: 369–377.Google Scholar
VARGAS, R.E., ALLRED, J.B., BIGGERT, M.D. and NABER, E.C. (1986) Effect of dietary 7-ketocholesterol, pure, or oxidized cholesterol on hepatic 3-hydroxy-3-methylglutaryl-coenzyme A reductase activity, energy balance, egg cholesterol concentration, and 14C-acetate incorporation into yolk lipids of laying hens. Poultry Science 65: 1333–1342.Google Scholar
VARGAS, R.E. and NABER, E.C. (1984) Relationship between dietary fiber and nutrient density and its effect on energy balance, egg yolk cholesterol and hen performance. Journal of Nutrition 114: 645–652.Google Scholar
WALDROUP, P.W., NDIFE, L.I., HELLWIG, H.M., HEBERT, J.A. and BERRIO, L. (1986) Influence of probucol ((4,4’-isopropylidine dithio)-bis(2,6-di-t-butyl-phenol)) on egg yolk cholesterol content and performance of laying hens. Poultry Science 65: 1949–1954.Google Scholar
WALZEM, R.L. (1996) Lipoproteins and the laying hen: Form follows function. Poultry and Avian Biology Reviews 7: 31–64.Google Scholar
WANG, J.-J. and PAN, T.-M. (2003) Effect of red mold rice supplements on serum and egg yolk cholesterol levels of laying hens. Journal of Agricultural and Food Chemistry 51: 4824–4829.Google Scholar
WASHBURN, K.W. (1979) Genetic variation in the chemical composition of the egg. Poultry Science 58: 529–535.Google Scholar
WASHBURN, K.W. and MARKS, H.L. (1977) Changes in fitness traits associated with selection for divergence in yolk cholesterol concentration. British Poultry Science 18: 189–199.Google Scholar
WEISS, F.G. and SCOTT, M.L. (1979) Effects of dietary fiber, fat and total energy upon plasma cholesterol and other parameters in chickens. Journal of Nutrition 109: 693–701.Google Scholar
WEISS, J.F., NABER, E.C. and JOHNSON, R.M. (1967) Effect of some dietary factors and drugs on cholesterol concentration in the egg and plasma of the hen. Journal of Nutrition 91: 119–128.CrossRefGoogle ScholarPubMed
WETTERAU, J.R., LIN, M.C.M. and JAMIL, H. (1997) Microsomal triglyceride transfer protein. Biochimica Biophysica Acta 1345: 136–150.Google Scholar
WIERZBICKI, A.S. (2003) New lipid-lowering agents. Expert Opinion on Emerging Drugs 8: 365–376.CrossRefGoogle ScholarPubMed
WIERZBICKI, A.S. (2004) Lipid-lowering therapies in development. Expert Opinion on Investigational Drugs 13: 1405–1418.Google Scholar
WOOD, D.L. and BITMAN, J. (1980) The effect of feeding di-(2-ethylhexyl) phthalate (DEHP) on the lipid metabolism of laying hens. Lipids 15: 151–156.CrossRefGoogle Scholar
WOOD, D.L. and BITMAN, J. (1984) The effect of feeding di-(2-ethylhexyl) phthalate and related compounds on lipids in the laying hen. Poultry Science 63: 469–477.CrossRefGoogle ScholarPubMed
WU, H., DWYER, K.M., FAN, Z., SHIRCORE, A., FAN, J. and DWYER, J.H. (2003) Dietary fiber and progression of atherosclerosis: The Los Angeles Atherosclerosis Study. American Journal of Clinical Nutrition 78: 1085–1091.CrossRefGoogle ScholarPubMed
YU, L., VON BERGMANN, K., LUTJOHANN, D., HOBBS, H.H. and COHEN, J.C. (2004) Selective sterol accumulation in ABCG5/ABCG8-deficient mice. Journal of Lipid Research 45: 301–307.CrossRefGoogle ScholarPubMed