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9 Cholesterol SUMMARY Cholesterol plays an important role in steroid hormone and bile acid biosynthesis and serves as an integral component of cell mem- branes. Given the capability of all tissues to synthesize sufficient amounts of cholesterol for their metabolic and structural needs, there is no evidence for a biological requirement for dietary cholesterol. Therefore, neither an Adequate Intake nor a Recom- mended Dietary Allowance is set for cholesterol. There is much evidence to indicate a positive linear trend between cholesterol intake and low density lipoprotein cholesterol concen- tration, and therefore increased risk of coronary heart disease (CHD). A Tolerable Upper Intake Level is not set for cholesterol because any incremental increase in cholesterol intake increases CHD risk. Because cholesterol is unavoidable in ordinary diets, eliminating cholesterol in the diet would require significant changes in patterns of dietary intake. Such significant adjustments may introduce undesirable effects (e.g., inadequate intakes of protein and certain micronutrients) and unknown and unquantifiable health risks. Nonetheless, it is possible to have a diet low in cholesterol while consuming a nutritionally adequate diet. Dietary guidance for minimizing cholesterol intake is provided in Chapter 11. 542
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543 C HOLESTEROL BACKGROUND INFORMATION Function Cholesterol is a sterol that is present in all animal tissues. Tissue choles- terol occurs primarily as free (unesterified) cholesterol, but is also bound covalently to fatty acids as cholesteryl esters and to certain proteins. Free cholesterol is an integral component of cell membranes and serves as a precursor for steroid hormones such as estrogen, testosterone, and aldosterone, as well as bile acids. Physiology of Absorption and Metabolism Absorption After emulsification and bile acid micellar solubilization, dietary choles- terol, as well as cholesterol derived from hepatic secretion and sloughed intestinal epithelium, is absorbed in the proximal jejunum. Cholesteryl esters, comprising 10 to 15 percent of total dietary cholesterol, are hydro- lyzed by a specific pancreatic esterase. Cholesterol absorption by enterocytes is believed to occur primarily by passive diffusion across a concentration gradient established by the solubilization of cholesterol in bile acid micelles. However, recent evidence has shown that scavenger receptor class B type I is present in the small intestine brush-border membrane where it facili- tates the uptake of micellar cholesterol (Hauser et al., 1998). In addition, as described further below, two recently identified adenosine triphosphate binding-cassette (ABC) proteins (ABCG5 and ABCG8) have been found to form heterodimers that export plant sterols and cholesterol from enterocytes into the gut lumen, thereby decreasing net sterol absorption (Berge et al., 2000). ABC1, a transporter involved in high density lipoprotein–(HDL) mediated cellular cholesterol efflux, may also participate in this process (Repa et al., 2000). Esterification of cholesterol and subsequent secretion of both esteri- fied and unesterified cholesterol into lymph and plasma in intestinally synthesized chylomicron and HDL particles may also affect net cholesterol uptake by enterocytes. Key components of this process include cholesterol esterification by acylCoA:cholesterol acyltransferase; lipoprotein assembly with the structural protein apoB48 (chylomicrons) and apoAI (HDL), as well as with triacylglycerols and phospholipids; and lipoprotein secretion into lymphatics facilitated by microsomal triacylglycerol transfer protein. Cholesterol balance studies in humans have indicated a wide variation in efficiency of intestinal cholesterol absorption (from 20 to 80 percent), with most individuals absorbing between 40 and 60 percent of ingested
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544 DIETARY REFERENCE INTAKES cholesterol (Ros, 2000). As discussed below, such variability, which is likely due in part to genetic factors, may contribute to interindividual differ- ences in plasma cholesterol response to dietary cholesterol. In addition, cholesterol absorption may be reduced by the cholesterol content of a meal and by decreased intestinal transit time (Ros, 2000). Although fatty acids are required for intestinal micelle formation, there is no strong evidence that fat content (or other dietary constituents such as fiber) has a significant effect on cholesterol absorption. An average of 250 mg/d of plant sterols (e.g., sitosterol, stigmasterol, and campesterol) are consumed in the diet, but the absorption of such sterols (approximately 5 percent) is considerably lower than that for cho- lesterol (Ling and Jones, 1995; Salen et al., 1970). They are not known to have important biological effects in humans at the levels consumed in the diet. An exception is sitosterolemia, a rare genetic disorder that is charac- terized by markedly increased absorption and tissue accumulation of plant sterols and elevated plasma cholesterol levels (Lütjohann et al., 1996; Salen et al., 1992). Recently, patients with this disorder have been shown to have mutations in genes encoding ABCG5 and ABCG8, indicating the impor- tance of these transporters in regulating sterol absorption presumably by promoting the export of nearly all plant sterols, and a portion of cholesterol, from intestinal cells (Berge et al., 2000). Moreover, increased expression of these genes induced by cholesterol feeding may be of importance in limiting cholesterol absorption (Berge et al., 2000). The ability of very high intakes of plant sterols to lower plasma cholesterol concentrations by reducing cholesterol absorption may also involve regulation of this trans- port process (Miettinen and Gylling, 1999). Metabolism Intestinally derived cholesterol is transported in the circulation to other tissues via chylomicrons, and to a lesser extent HDL, mainly in the form of cholesteryl ester. The hydrolysis of chylomicron triacylglycerols in peripheral tissues by lipoprotein lipase and subsequent remodeling by lipid transfer proteins yields a “remnant” particle that is internalized by receptors, primarily in the liver, that recognize apoprotein E and perhaps other con- stituents. Cholesterol released by intracellular cholesteryl esterase activity can be stored in hepatocytes; re-esterified and secreted into plasma in lipoproteins, primarily very low density lipoproteins (VLDL); oxidized and excreted as bile acids; or directly secreted into the bile. Free and esterified cholesterol circulate in the blood in humans principally in low density lipoproteins (LDL). Cholesterol homeostasis in hepatocytes is of critical importance for the regulation of plasma LDL cholesterol concentrations (Dietschy et al.,
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545 C HOLESTEROL 1993). Increased cellular cholesterol content leads to suppression of syn- thesis of LDL receptors via a series of steps resulting in interaction of sterol regulatory element-binding protein (SREBP) 1 and 2 transcription factors with a sterol response element in the LDL receptor gene (Brown and Goldstein, 1999). Increased plasma LDL concentrations can result from reduced hepatic LDL uptake, as well as reduced uptake of VLDL and intermediate density lipoproteins, leading to increased metabolic conver- sion of these particles to LDL (Kita et al., 1982). Metabolic studies in humans have indicated that a high cholesterol diet induces both increased LDL synthesis and reduced receptor-dependent fractional removal rate of LDL particles (Packard et al., 1983). There are a number of other genes involved in cholesterol and lipo- protein metabolism in which hepatic regulation can be affected by choles- terol availability either directly via SREBPs or indirectly by the action of other transcription factors, such as liver X receptors (Repa and Mangelsdorf, 2000). These genes play a role in cholesterol regulatory pathways, including those involved in cholesterol synthesis that are suppressed by cholesterol (e.g., 3-hydroxy-3-methylglutaryl coenzyme A [HMG CoA] reductase) and others involved in bile acid production from cholesterol that are activated by cholesterol (e.g., 7 α-hydroxylase). Thus, increased hepatic cholesterol delivery from diet and other sources results in a complex admixture of metabolic effects that are generally directed at maintaining tissue and plasma cholesterol homeostasis. However, as described below, empirical observations in humans have indicated that increased dietary cholesterol does result in a net increase in plasma LDL cholesterol concentrations, probably as a consequence of reduced hepatic LDL receptor activity. All cells are capable of synthesizing cholesterol in sufficient amounts for their structural and metabolic needs. However, certain tissues (e.g., adrenal glands and gonads) derive a significant proportion of cholesterol by uptake from plasma lipoproteins. Cholesterol synthesis via a series of intermediates from acetyl CoA is highly regulated. The enzyme HMG CoA reductase catalyzes the rate-limiting step in cholesterol synthesis—the for- mation of mevalonic acid from HMG CoA. The genes for this enzyme and a number of other proteins involved in cholesterol metabolism, such as the LDL receptor, are regulated by intracellular sterols and other signal- ing molecules to maintain tissue cholesterol homeostasis, as described above. Endogenous cholesterol synthesis in humans is approximately 12 to 13 mg/kg/d (840 to 910 mg/d for a 70-kg individual) (Di Buono et al., 2000). Another group of diet-derived sterols with potential biological effects are oxysterols (Vine et al., 1998), which are cholesterol oxidation products that can be found in cholesterol-rich processed foods such as dried egg yolk, although typical levels of oxysterols in the diet are generally low
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546 DIETARY REFERENCE INTAKES (van de Bovenkamp et al., 1988). These cholesterol oxidation products can have major effects on cholesterol metabolism and have been shown to be highly atherogenic in animal models (Staprans et al., 2000; Vine et al., 1998). Their role in human nutrition remains to be established. Overall, body cholesterol homeostasis is highly regulated by balancing intestinal absorption and endogenous synthesis with hepatic excretion of cholesterol and bile acids derived from hepatic cholesterol oxidation. FINDINGS BY LIFE STAGE AND GENDER GROUP Given the capability of all tissues to synthesize sufficient cholesterol for their metabolic and structural needs, there is no evidence for a biologi- cal requirement for dietary cholesterol. As an example, many Tarahumara Indians of Mexico consume very low amounts of dietary cholesterol and have no reported developmental or health problems that could be attrib- uted to this aspect of their diet (McMurry et al., 1982). Therefore, neither an Adequate Intake (AI) nor an Estimated Average Requirement (EAR) and Recommended Dietary Allowance (RDA) are set for cholesterol. The question of whether cholesterol in the infant diet plays some essential role on lipid and lipoprotein metabolism that is relevant to growth and development or to the atherosclerotic process in adults has been diffi- cult to resolve. The idea that the early diet might have relevance to later lipid metabolism was first raised by Hahn and Koldovsky (1966) in pre- ´ maturely weaned rat pups and later supported by observations that normal weaning to a high intake of cholesterol resulted in greater resistance to dietary cholesterol in later adulthood (Reiser and Sidelman, 1972; Reiser et al., 1979). This led to the hypothesis that cholesterol in human milk may play some important role in establishing regulation of cholesterol homeostasis. Since human milk typically provides about 100 to 200 mg/L (Table 9-1), whereas infant formulas contain very little cholesterol (10 to 30 mg/L) (Huisman et al., 1996; Wong et al., 1993), it is not surprising that plasma cholesterol concentrations are higher in infants fed human milk than in formula-fed infants. Formula-fed infants also have a higher rate of cholesterol synthesis (Bayley et al., 1998; Cruz et al., 1994; Wong et al., 1993). However, the available evidence suggests that this effect is tran- sient. Differences in cholesterol synthesis and plasma cholesterol concen- tration are not sustained once complementary feeding is introduced (Darmady et al., 1972; Friedman and Goldberg, 1975; Mize et al., 1995). Also, no clinically significant effects on growth and development due to these differences in plasma cholesterol concentration have been noted between breast-fed and formula-fed infants under 1 year of age. One explanation may be that the developing brain synthesizes the cholesterol required for myelination in situ and does not take up cholesterol from
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547 C HOLESTEROL TABLE 9-1 Cholesterol Content in Term Human Milk of Women in the United States Reference Stage of Lactation Cholesterol Content (mg/L) n Picciano et al., 18 6–12 wk postpartum 1978 (pp) Early morning 157 Midday 151 Evening 178 Mellies et al., 33 1 mo pp 201 1979 2 mo pp 195 3 mo pp 97 4 mo pp 220 5 mo pp 156 6 mo pp 283 7 mo pp 289 8 mo pp 220 9 mo pp 260 10 mo pp 210 11 mo pp 135 12–13 mo pp 151 Clark et al., 10 2 wk pp 110 1982 6 wk pp 97 12 wk pp 103 16 wk pp 104 Bitman et al., 6 3 wk pp 122 1983 6 wk pp 112 12 wk pp 103 Lammi-Keefe et al., 6 8 wk pp 1990 0600 h 88 1000 h 107 1400 h 111 1800 h 110 2200 h 112 Jensen et al., 10 12 wk pp 1995 0600–1000 h 140 1000–1400 h 162 1400–1800 h 217 1800–2200 h 220 2200–0600 h 129 Bayley et al., 14 4 mo pp 120 1998
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548 DIETARY REFERENCE INTAKES plasma (Edmond et al., 1991; Haave and Innis, 2001; Jurevics and Morell, 1994). The effects of early cholesterol intake and weaning on cholesterol metabolism later in life have been studied in a number of different animal species (Hamosh, 1988; Kris-Etherton et al., 1979; Mott et al., 1990) and in short-term studies with infants and children. Studies in baboons fed breast milk or formulas with or without cholesterol and with varying fat composi- tions found that early cholesterol intake had little effect on serum choles- terol concentrations in young adults up to about 8 years of age (Mott et al., 1990). However, adult baboons that had been breast fed had lower high density lipoprotein (HDL) cholesterol concentrations, higher very low density lipoprotein + low density lipoprotein (LDL):HDL ratios, and more extensive atherosclerotic lesions than those that had been formula fed (Lewis et al., 1988; Mott et al., 1990, 1995). These differences were not explained by variations in the saturated and unsaturated fat content of the formulas and milk. The major metabolic difference associated with the differences in plasma lipoproteins was lower rates of bile acid synthesis and excretion among the baboons that had been breast fed. The possible relations of early breast and bottle feeding with later cholesterol concentrations and other coronary heart disease risk factors were explored in several short-term studies and larger retrospective epide- miological studies, but these observations are inconsistent (Fall et al., 1992; s Kolacek et al., 1993; Leeson et al., 2001; Ravelli et al., 2000). The relationship between early dietary cholesterol intake from milk or formula and serum cholesterol concentration in infancy and that observed in children and young adults following their usual diets was either absent (Andersen et al., 1979; Friedman and Goldberg, 1975; Glueck et al., 1972; Huttunen et al., 1983), in favor of formula feeding compared to breast feeding during infancy in 7- to 12-year-old children (Hodgson et al., 1976), or in favor of feeding human milk compared to formula feeding in men and women. The disparate findings may be due to confounding factors such as duration of breast feeding, since human-milk feeding for less than 3 months was associated with higher serum cholesterol concentrations in men at 18 to 23 years of age, or the type of formula fed since formula composition, especially quality of fat, which has changed dramatically in s the last century (Kolacek et al., 1993). A follow-up study of nearly 6,000 elderly men for whom early feeding methods had been recorded found higher total and LDL cholesterol concentrations and increased risk of coronary heart disease (CHD) mortality in men who had been exclusively fed human milk than in those who had been fed human milk and bottle fed or fed human milk and weaned at 1 year of age. Men who had been exclusively bottle-fed during infancy also had higher total and LDL choles-
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549 C HOLESTEROL terol concentrations and CHD mortality than men who had previously been fed human milk (Fall et al., 1992). The available data do not warrant a recommendation with respect to dietary cholesterol intake for infants who are not fed human milk. How- ever, further research to identify possible mechanisms whereby early nutri- tional experiences affect the atherosclerotic process in adults, as well as the sensitive periods in development when this may occur, would be valuable. INTAKE OF CHOLESTEROL Food Sources Cholesterol is present in foods of animal origin. High amounts of cholesterol are present in liver (375 mg/3 oz slice) and egg yolk (250 mg/ yolk). Although generally low in total fat, some seafood, including shrimp, lobster, and certain fish, contain moderately high amounts of cholesterol (60 to 100 g/half-cup serving). One cup of whole milk contains approxi- mately 30 mg of cholesterol, whereas the cholesterol contained in 2 per- cent and skim milk is 15 and 7 mg/cup, respectively. Therefore, products that contain milk (e.g., cheese, ice cream, and cottage cheese) are moderate sources of cholesterol. One tablespoon of butter contains approximately 12 mg of cholesterol, whereas margarine does not contain cholesterol. The majority of cholesterol is consumed from eggs and meat (FASEB, 1995). Dietary Intake Based on intake data from the Continuing Survey of Food Intakes by Individuals (1994–1996, 1998), the median cholesterol intake ranged from approximately 250 to 325 mg/d for men and 180 to 205 mg/d for women (Appendix Table E-15). ADVERSE EFFECTS OF OVERCONSUMPTION Hazard Identification Plasma Total, HDL, and LDL Cholesterol Concentrations Numerous studies in humans have examined the effects of dietary cholesterol on plasma total and lipoprotein cholesterol concentrations (Tables 9-2 and 9-3, Figures 9-1 and 9-2), and empirical formulas have been derived to describe these relationships. Although most studies have
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550 DIETARY REFERENCE INTAKES TABLE 9-2 Effects of Adding Dietary Cholesterol to Defined Diets with Strict Control of Dietary Intake on Serum Cholesterol Concentration Baseline Dietary Added Dietary Cholesterol Cholesterol Reference (mg/d) (mg/d) n Beveridge et al., 6 13 81 1960 9 13 140 9 13 280 9 13 621 6 13 1,282 10 13 2,481 9 13 4,490 Connor et al., 2 0 475 1961a 2 0 950 2 0 1,425 Connor et al., 3 0 2,400 1961b 1 0 1,650 1 0 1,900 1 0 4,800 Steiner et al., 1962 6 0 3,000 Wells and Bronte- 3 0 17 Stewart, 1963 3 0 42 3 0 67 3 0 88 3 0 142 3 0 267 3 0 517 3 0 1,017 3 0 1,517 3 0 3,017 Connor et al., 1964 6 0 729 5 0 725 Erickson et al., 6 0 742 1964 6 0 742 Hegsted et al., 1965 10 116 570 10 306 380 10 116 570
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551 C HOLESTEROL Change in Serum Total Percent of Cholesterol Calories from (mmol/L) Fat P:S Ratio 0.06 30 0.08 0.10 30 0.08 1.17 30 0.08 0.43 30 0.08 0.59 30 0.08 1.20 30 0.08 0.87 30 0.08 1.71 40 0.76 1.64 40 0.76 1.99 40 0.76 1.47 40 0.88 2.43 40 0.88 2.97 40 0.88 2.53 40 0.88 1.30 40 0.68 0.44 15 0.56 15 0.66 15 0.80 15 0.96 15 1.03 15 1.18 15 1.09 15 1.29 15 1.23 15 1.03 40 0.25 0.74 40 1.7 0.61 41 1.6 0.69 41 1.6 0.75 39 5.4 0.29 39 0.05 0.70 39 0.68 continued
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552 DIETARY REFERENCE INTAKES TABLE 9-2 Continued Baseline Dietary Added Dietary Cholesterol Cholesterol Reference (mg/d) (mg/d) n Keys et al., 1965 22 50 470 22 50 1,410 22 50 33 22 50 1,400 22 50 1,410 National Diet-Heart 81 126 495 Study Research 81 126 495 Group,1968 57 401 495 57 154 495 Quintão et al., 1971 4 43 2,441 1 43 499 1 44 197 2 53.5 4,002 Mattson et al., 1972 14 0 297 14 0 594 14 0 888 Anderson et al., 12 3 291 1976 12 3 291 Nestel and Poyser, 4 210 500 1976 2 257 500 2 334 532 1 103 439 Quintão et al., 1977 6 0 3,250 Bronsgeest-Schoute 21 98 567 et al., 1979a, 21 98 567 1979b 9 124 607 9 124 607 Lin and Connor, 2 45 1,081 1980 McMurry et al., 12 0 600 1981
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578 DIETARY REFERENCE INTAKES TABLE 9-8 Dietary Cholesterol and Risk of Prostate Cancer Reference Study Design Dietary and Other Information Kolonel et al., 452 cases Dietary history 1988 899 controls Adjusted for age Case-control and ethnicity Andersson 522 cases Food frequency et al., 1996 536 controls questionnaire Case-control Adjusted for age and energy Key et al., 328 cases Food frequency 1997 328 controls questionnaire Case-control Vlajinac et al., 101 cases Dietary history 1997 202 controls Adjusted for energy Case-control and significant nutrients a OR = odds ratio. • Other factors (dietary and constitutional) that contribute to the wide interindividual variation in LDL cholesterol response to dietary cholesterol also need to be delineated. • Studies are needed to better define the relation between dietary cholesterol intakes and LDL cholesterol concentrations over a broad range of cholesterol intakes, from very low to high. • The relationship between dietary cholesterol intakes and body pools of cholesterol needs to be determined. REFERENCES Alavanja MCR, Brown CC, Swanson C, Brownson RC. 1993. Saturated fat intake and lung cancer risk among nonsmoking women in Missouri. J Natl Cancer Inst 85:1906–1916. Andersen GE, Lifschitz C, Friis-Hansen B. 1979. Dietary habits and serum lipids during first 4 years of life. A study of 95 Danish children. Acta Paediatr Scand 68:165–170.
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579 C HOLESTEROL Resultsa Comments Age and OR for Significant positive Quartile of cholesterol prostate cancer association between < 70 ≥ 70 intake cholesterol intake and 1 (low) 1.0 1.0 risk of prostate cancer, 2 1.2 1.6 but no clear gradient 3 1.2 1.7 effect 4 (high) 1.3 1.6 Cholesterol intake (mg/d) OR for prostate cancer No association between < 241 1.00 cholesterol intake and 241–301 0.71 risk of prostate cancer 302–390 0.85 > 390 0.96 Mean cholesterol intake No significant difference (mg/d) in cholesterol intake Cases 341 between prostate Controls 351 cancer cases andcontrols Tertile of cholesterol intake OR for prostate cancer No significant association 1 1.00 between cholesterol 2 0.97 intake and risk of 3 0.60 prostate cancer Anderson JT, Grande F, Keys A. 1976. Independence of the effects of cholesterol and degree of saturation of the fat in the diet on serum cholesterol in man. Am J Clin Nutr 29:1184–1189. Andersson S-O, Wolk A, Bergström R, Giovannucci E, Lindgren C, Baron J, Adami H-O. 1996. Energy, nutrient intake and prostate cancer risk: A population- based case-control study in Sweden. Int J Cancer 68:716–722. Applebaum-Bowden D, Haffner SM, Hartsook E, Luk KH, Albers JJ, Hazzard WR. 1984. Down-regulation of the low-density lipoprotein receptor by dietary cho- lesterol. Am J Clin Nutr 39:360–367. Ascherio A, Rimm EB, Giovannucci EL, Spiegelman D, Stampfer M, Willett WC. 1996. Dietary fat and risk of coronary heart disease in men: Cohort follow up study in the United States. Br Med J 313:84–90. Bayley TM, Alasmi M, Thorkelson T, Krug-Wispe S, Jones PJH, Bulani JL, Tsang RC. 1998. Influence of formula versus breast milk on cholesterol synthesis rates in four-month-old infants. Pediatr Res 44:60–67. Berge KE, Tian H, Graf GA, Yu L, Grishin NV, Schultz J, Kwiterovich P, Shan B, Barnes R, Hobbs HH. 2000. Accumulation of dietary cholesterol in sitosterolemia caused by mutations in adjacent ABC transporters. Science 290:1771–1775.
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580 DIETARY REFERENCE INTAKES Beveridge JMR, Connell WF, Mayer GA, Haust HL. 1960. The response of man to dietary cholesterol. J Nutr 71:61–65. Beynen AC, Katan MB. 1985a. Effect of egg yolk feeding on the concentration and composition of serum lipoproteins in man. Atherosclerosis 54:157–166. Beynen AC, Katan MB. 1985b. Reproducibility of the variations between humans in the response of serum cholesterol to cessation of egg consumption. Athero- sclerosis 57:19–31. Bitman J, Wood L, Hamosh M, Hamosh P, Mehta NR. 1983. Comparison of the lipid composition of breast milk from mothers of term and preterm infants. Am J Clin Nutr 38:300–312. Bocan TMA. 1998. Animal models of atherosclerosis and interpretation of drug intervention studies. Curr Pharm Des 4:37–52. Bronsgeest-Schoute DC, Hautvast JGAJ, Hermus RJJ. 1979a. Dependence of the effects of dietary cholesterol and experimental conditions on serum lipids in man. I. Effects of dietary cholesterol in a linoleic acid-rich diet. Am J Clin Nutr 33:2183–2187. Bronsgeest-Schoute DC, Hermus RJJ, Dallinga-Thie GM, Hautvast JGAJ. 1979b. Dependence of the effects of dietary cholesterol and experimental conditions on serum lipids in man. II. Effects of dietary cholesterol in a linoleic acid-poor diet. Am J Clin Nutr 33:2188–2192. Brown MS, Goldstein JL. 1999. A proteolytic pathway that controls the cholesterol content of membranes, cells, and blood. Proc Natl Acad Sci USA 96:11041– 11048. Byers TE, Graham S, Haughey BP, Marshall JR, Swanson MK. 1987. Diet and lung cancer risk: Findings from the Western New York Diet Study. Am J Epidemiol 125:351–363. Clark RM, Ferris AM, Fey M, Brown PB, Hundrieser KE, Jensen RG. 1982. Changes in the lipids of human milk from 2 to 16 weeks postpartum. J Pediatr Gastroenterol Nutr 1:311–315. Clarke R, Frost C, Collins R, Appleby P, Peto R. 1997. Dietary lipids and blood cholesterol: Quantitative meta-analysis of metabolic ward studies. Br Med J 314:112–117. Clifton PM, Kestin M, Abbey M, Drysdale M, Nestel PJ. 1990. Relationship between sensitivity to dietary fat and dietary cholesterol. Arteriosclerosis 10:394–401. Clifton PM, Abbey M, Noakes M, Beltrame S, Rumbelow N, Nestel PJ. 1995. Body fat distribution is a determinant of the high-density lipoprotein response to dietary fat and cholesterol in women. Arterioscler Thromb Vasc Biol 15:1070–1078. Connor WE, Hodges RE, Bleiler RE. 1961a. Effect of dietary cholesterol upon serum lipids in man. J Lab Clin Med 57:331–342. Connor WE, Hodges RE, Bleiler RE. 1961b. The serum lipids in men receiving high cholesterol and cholesterol-free diets. J Clin Invest 40:894–901. Connor WE, Stone DB, Hodges RE. 1964. The interrelated effects of dietary choles- terol and fat upon human serum lipid levels. J Clin Invest 43:1691–1696. Cruz MLA, Wong WW, Mimouni F, Hachey DL, Setchell KDR, Klein PD, Tsang RC. 1994. Effects of infant nutrition on cholesterol synthesis rates. Pediatr Res 35:135–140. Darmady JM, Fosbrooke AS, Lloyd JK. 1972. Prospective study of serum cholesterol levels during first year of life. Br Med J 2:685–688. Di Buono M, Jones PJH, Beaumier L, Wykes LJ. 2000. Comparison of deuterium incorporation and mass isotopomer distribution analysis for measurement of human cholesterol biosynthesis. J Lipid Res 41:1516–1523.
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Representative terms from entire chapter: