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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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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.
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Representative terms from entire chapter:
cholesterol intake
