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Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids
9
Cholesterol
SUMMARY
Cholesterol plays an important role in steroid hormone and bile acid biosynthesis and serves as an integral component of cell membranes. 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 Recommended Dietary Allowance is set for cholesterol.
There is much evidence to indicate a positive linear trend between cholesterol intake and low density lipoprotein cholesterol concentration, 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.
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BACKGROUND INFORMATION
Function
Cholesterol is a sterol that is present in all animal tissues. Tissue cholesterol 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 cholesterol, 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 hydrolyzed 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 facilitates 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 esterified 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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cholesterol (Ros, 2000). As discussed below, such variability, which is likely due in part to genetic factors, may contribute to interindividual differences 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 cholesterol (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 characterized 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 importance 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 transport 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 constituents. 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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1993). Increased cellular cholesterol content leads to suppression of synthesis 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 conversion 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 lipoprotein metabolism in which hepatic regulation can be affected by cholesterol 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 formation 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 signaling 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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(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 biological 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 attributed 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 difficult to resolve. The idea that the early diet might have relevance to later lipid metabolism was first raised by Hahn and Koldovský (1966) in prematurely 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 transient. Differences in cholesterol synthesis and plasma cholesterol concentration 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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TABLE 9-1 Cholesterol Content in Term Human Milk of Women in the United States
Reference
n
Stage of Lactation
Cholesterol Content (mg/L)
Picciano et al., 1978
18
6–12 wk postpartum (pp)
Early morning
157
Midday
151
Evening
178
Mellies et al., 1979
33
1 mo pp
201
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., 1982
10
2 wk pp
110
6 wk pp
97
12 wk pp
103
16 wk pp
104
Bitman et al., 1983
6
3 wk pp
122
6 wk pp
112
12 wk pp
103
Lammi-Keefe et al., 1990
6
8 wk
pp
0600 h
88
1000 h
107
1400 h
111
1800 h
110
2200 h
112
Jensen et al., 1995
10
12 wk
pp
0600–1000 h
140
1000–1400 h
162
1400–1800 h
217
1800–2200 h
220
2200–0600 h
129
Bayley et al., 1998
14
4 mo pp
120
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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 compositions found that early cholesterol intake had little effect on serum cholesterol 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 epidemiological studies, but these observations are inconsistent (Fall et al., 1992; Kolaček 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 the last century (Kolaček 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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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. However, further research to identify possible mechanisms whereby early nutritional 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 approximately 30 mg of cholesterol, whereas the cholesterol contained in 2 percent 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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TABLE 9-2 Effects of Adding Dietary Cholesterol to Defined Diets with Strict Control of Dietary Intake on Serum Cholesterol Concentration
Reference
n
Baseline Dietary Cholesterol (mg/d)
Added Dietary Cholesterol (mg/d)
Beveridge et al., 1960
6
13
81
9
13
140
9
13
280
9
13
621
6
13
1,282
10
13
2,481
9
13
4,490
Connor et al., 1961a
2
0
475
2
0
950
2
0
1,425
Connor et al., 1961b
3
0
2,400
1
0
1,650
1
0
1,900
1
0
4,800
Steiner et al., 1962
6
0
3,000
Wells and Bronte-Stewart, 1963
3
0
17
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., 1964
6
0
742
6
0
742
Hegsted et al., 1965
10
116
570
10
306
380
10
116
570
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Change in Serum Total Cholesterol (mmol/L)
Percent of Calories from 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
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Reference
n
Baseline Dietary Cholesterol (mg/d)
Added Dietary Cholesterol (mg/d)
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 Study Research Group,1968
81
126
495
81
126
495
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., 1976
12
3
291
12
3
291
Nestel and Poyser, 1976
4
210
500
2
257
500
2
334
532
1
103
439
Quintão et al., 1977
6
0
3,250
Bronsgeest-Schoute et al., 1979a, 1979b
21
98
567
21
98
567
9
124
607
9
124
607
Lin and Connor, 1980
2
45
1,081
McMurry et al., 1981
12
0
600
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TABLE 9-8 Dietary Cholesterol and Risk of Prostate Cancer
Reference
Study Design
Dietary and Other Information
Kolonel et al., 1988
452 cases
899 controls
Case-control
Dietary history
Adjusted for age and ethnicity
Andersson et al., 1996
522 cases
536 controls
Case-control
Food frequency questionnaire
Adjusted for age and energy
Key et al., 1997
328 cases
328 controls
Case-control
Food frequency questionnaire
Vlajinac et al., 1997
101 cases
202 controls
Case-control
Dietary history
Adjusted for energy 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.
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Resultsa
Comments
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Age and OR for prostate cancer
Significant positive association between cholesterol intake and risk of prostate cancer, but no clear gradient effect
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1.00
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0.85
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Mean cholesterol intake (mg/d)
No significant difference in cholesterol intake between prostate cancer cases andcontrols
Cases
341
Controls
351
Tertile of cholesterol intake
OR for prostate cancer
No significant association between cholesterol intake and risk of prostate cancer
1
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Representative terms from entire chapter:
cholesterol intake
