Variability in Response to a Low-Fat, Low-Cholesterol Diet in Children with Elevated Low-Density Lipoprotein Cholesterol Levels

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Variability

in Response

to a Low-Fat,

Low-Cholesterol

Diet

in Children

with

Elevated

Low-Density

Lipoprotein

Cholesterol

Levels

Eric S. Quivers, MD*; David

J.

Driscoll, MDC; Colleen D. Garvey;

Ann M. Harrist; Jay Harrison, MSII; Diane M. Huse, MS;

Paul Murtaugh, PhDII; and William H. Weidman, MD*

ABSTRACT. The reduction of dietary cholesterol and fat lowers low-density lipoprotein cholesterol (LDL-C) and reduces risk of coronary heart disease in adults. The

purpose of this study was to determine the individual variability of response of serum lipid and lipoprotein levels to a low-fat, low-cholesterol diet in children with elevated LDL-C levels. Thirty-two children (2 to 16 years of age) enrolled in a diet modification program, who had LDL-C levels of at least 110 mg/dL but normal triglyc-eride levels for their ages, were studied. Lipid levels and dietary nutrients were analyzed at the time of admission, and final assessments were made at least 3 months after entry. There was a significant correlation, for the group as a whole, between change in LDL-C concentration and change in grams of dietary saturated fat; however, there was marked individual variability in LDL-C response. There were no significant correlations between changes in LDL-C levels and changes in either total fat, polyun-saturated fat, or cholesterol intake. It is concluded that modest decreases in dietary saturated fat coincide with a lowering of LDL-C concentration, over a short term, in many children, but the degree of lowering varies consid-erably from one child to another. This variability is consistent with the concept that response of serum lipid levels to dietary changes is modified by genetic, meta-bolic, and other, as of yet, undefined variables. Pediatrics

1992;89:925-929; low-density lipoprotein cholesterol, die-tary saturated fat, variable response.

ABBREVIATIONS. LDL-C, low-density lipoprotein cholesterol; HDL-C, high-density lipoprotein cholesterol; NS, not significant.

Atherosclerosis, or its precursors, begins in

child-hood.’3 There is evidence that increased levels of

serum cholesterol, particularly low-density lipopro-tein cholesterol (LDL-C), are responsible, in a large part, for the development of atherosclerosis.45 Chil-dren in the United States have higher levels of blood

cholesterol than do children in countries where the

incidence of coronary heart disease in adults is low.6’7

In addition, children with high serum cholesterol

levels have an increased risk of having high levels

subsequently as adults.8 Evidence strongly suggests that lowering blood cholesterol levels in children will

* From the Section of Pediatric Cardiology, Cardiovascular Health Clinic for the Young, §Department of Nutrition, and IlSection of Medical Statistics,

Mayo Clinic, Rochester, MN. Dr Quivers is a fellow of the Mayo Clinic.

Received for publication Jun 22, 1990; accepted Aug 26, 1991.

Reprint requests to (D.J.D.) Pediatric Cardiology, Mayo Clinic, Rochester,

MN 55905.

PEDIATRICS (lSSN 0031 4005). Copyright ‘i) 1992 by the American Acad-emy of Pediatrics.

reduce their risk of coronary heart disease during

adulthood. The first strategy to lower lipid levels in American children is the development of nutritional habits that include the limitation of dietary fat to 30%

of calories, with no more than 10% from saturated

fat, up to 10% from polyunsaturated fat, the

remain-der from monosaturated fat, and less than 300 mg of

cholesterol per day (American Heart Association and

National Cholesterol Education Program Step 1 Diet). It is important to know what effect can be expected.

The response of plasma lipid levels to change in

dietary nutrients has been studied mostly in adults, with fewer studies in children. Almost all published

studies suffer from the same problems. Most studies

of the response of serum lipid levels, in adults, to

dietary nutrients have focused on average effects and

present only mean Other reports have been

of small groups studied under tightly controlled

en-vironments.12’4 Jacobs et al’5 studied 58 mentally

retarded, institutionalized males. The actual response of serum cholesterol level to diets low in saturated fat

was related to the expected response based on the

Keys-Minnesota equation. Eighty-two percent

re-sponded within 50% of predicted, 9% were

hypores-ponders, and another 9% were hyperresponders.

McGandy et al’6 and Stein et al’7 reported the

re-sponse of serum cholesterol levels, in adolescent

males, to diets high in polyunsaturated fat. The

de-crease in serum cholesterol concentration was slightly

less in those with admission levels equal to or less

than 199 mg/dL than in those with levels equal to or

exceeding 200 mg/dL. However, as in many of the

adult studies, only mean values were given, individ-ual baseline and response levels were not presented, and the possibility that regression to the mean could have been partly responsible for these differences

was not addressed. Other reports concerning dietary

changes and effect on serum cholesterol and LDL-C

levels in children have also presented only mean

values.’82#{176} In two studies21’22 only mean lipid level

changes were reported. The authors stated that

dif-ferences in baseline dietary fat and cholesterol2’ or

baseline levels of total and LDL-C22 effected response. Neither study presented a statistical analysis of

in-dependent factors effecting response of blood lipid

levels.

Individual baseline blood levels and the

corre-sponding response levels are rarely presented, and

there are no frequency distributions of the responses.

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im-Dietary Variables Average calories Total fat, g

%Calories from total

TABLE 1. Nutrition and Blood Lipid Assessment

SD 363.54 15.91 5.73 CV* 0.25 0.32 0.20 Average (Range) Mean (Range) 1475.47 (841-2437) 48.43 (16-86) 29.35 (12.3-40.2) 14.84 (4.0-28.0) 9.03 (3.4-14.2) 6.74 (1.6-19.0) 4.24 (1.4-11.7) 132.46 (19-234) 201.84 (162-329) 147.69 (114.8-284.2) 44.81 (33-59) 59.71 (24-115) 5,39 0.36 2.34 0.26 3.63 0.54 2.52 0.59 63.78 0.48 31.18 32.83 7.79 23.60 0.15 0.22 0.17 0.40

portant in the evaluation of the effect of dietary

changes on a population as is the average response.

When investigators at the Mayo Clinic opened the

Cardiovascular Health Clinic for the Young in 1987,

a protocol was developed to allow evaluation of the

nutritional management of children and adolescents

with hyperlipidemia. The present study was done to

evaluate the short-term (3 to 40 months) effectiveness

of dietary management, using the Step 1 Diet, in

children with serum LDL-C levels above 1 10 mg/dL

(75th percentile) and normal total triglyceride levels (less than the 95th percentile for age).

MATERIALS AND METHODS

From the 259 patients enrolled in the Cardiovascular Health Clinic for the Young between 1986 and 1989, we selected a subgroup of 32 patients (2 to 16 years of age) having (1) two initial LDL-C values of at least 1 10 mg/dL; (2) normal triglyceride levels for their age groups (initial triglyceride levels <100 mg/dL for 2-through 9-year-old children, <129 mg/dL for 10- through 14-year-olds, and <152 mg/dL for 15- to 16-year-olds); (3) at least 90 days of participation in the study; (4) at least three lipid and lipoprotein measurements; and (5) at least two nutritional assessments. The majority of the patients had lipid levels measured because of a family history of hyperlipidemia and/or premature vascular dis-ease. Of the admission lipid measurements, the one closest to the diet evaluation was used; there was an average of 1 1 days between this lipid measurement and the first nutritional assessment, and 5 days between the last lipid measurement and last nutritional as-sessment (Table 1). Lipid measurements preceded nutritional as-sessments. These 32 patients (16 female, 16 male) were enrolled between March 26, 1987, and September 7, 1989, and had a median

time on study of 401 days (range, 137 to 1195 days). The rationale for selecting this subgroup was to limit the cohort to one with

LDL-Celevation only so that very-low-density lipoprotein abnormalities

in some, but not others, would not complicate interpretation of

dietary response of LDL-C.

The admission and follow-up lipid and lipoprotein levels and dietary nutrients were compared with Wilcoxon signed-rank tests. Relationships between the changes in LDL-C levels and changes in dietary variables were examined with Spearman rank

correla-tions.

The evaluation and management of these patients was per-formed in a uniform fashion by a team consisting of two pediatric cardiologists, three pediatric registered dietitians, and a clinic co-ordinator. During the initial visit, a complete medical history and a detailed family history with particular reference to hyperlipidemia, obesity, diabetes, hypertension, stroke, and myocardial infarction were obtained. All patients had a physical examination; remea-surement of serum levels of total cholesterol, triglycerides, high-density lipoprotein cholesterol (HDL-C), thyroxine, sodium, potas-sium, serum protein, albumin, bilirubin, aspartate aminotrans-ferase, and creatinine; and urinalysis. Total cholesterol, total tn-glyceride, sodium, potassium, protein, albumin, bilirubin, aspartate aminotransferase, and creatinine levels were measured enzymati-cally using the Hitachi 717 analyzer. High-density lipoprotein cholesterol was measured by selective precipitation with dextran

No. of lipid measurements 4 (2-8)

Days between first and last lipid 444 (137-1195)

measurements

No. of nutritional assessments 3 (2-6)

Days between first and last nutn- 437 (1 19-1176) tional assessments

Days between first laboratory visit I 1 (0-3 1) and first nutritional assessment

Days between last lipid measure- 5 (0-1 1) .

ment and last nutritional

assess-ment

sulfate and calcium chloride. Low-density lipoprotein cholesterol was calculated using the Friedewald formula (LDL-C = total cho-lesterol - HDL-C - total triglycerides -‘- 5). The patient and family

were instructed to maintain a prospective 3- to 5-day dietary history (including only one weekend day). Three weeks after the initial visit, the results of laboratory tests and the dietary history were reviewed with the family and initial dietary instruction was

pro-vided. Dietary nutrients were estimated using the Nutritionist III Computer Program. Depending on the patient’s age, several aids to dietary modification were employed to simplify adherence to dietary alterations. Subsequently, dietary counseling was per-formed 6, 12, 18, 24, 30, 36, 42, 48, and 52 weeks after the initial

visit and subsequently every 3 to 6 months. Serum lipid and

lipoprotein levels, height, weight, blood pressure, and hip and waist measurements were obtained about 12, 30, and 48 weeks after the initial visit and every 6 months thereafter. Prospective 3-to 5-day diet diaries also were obtained at the time of the lipid measurements (Table 1).

The goal of the dietary modification was to provide a Step I Diet: 30% of calories from fat, less than 10% from saturated fat, no more than 10% from polyunsaturated fat, and the remainder from monosaturated fat; dietary cholesterol less than 300 mg/d; and adequate caloric intake for growth, physical activity, and maintenance of normal weight. The primary tool in teaching the concept of the fat/cholesterol content of foods was a multicolored graphic display giving the relative fat content of a variety of common and popular foods. This diagram illustrated how the fat content of food can change by method of food preparation and gave ideas for substituting lower for higher fat foods. The child was encouraged to use this diagram daily for help with food selection. The child was not told that he or she must avoid any food (including foods containing saturated fat and cholesterol). He or she was told that all foods were acceptable but their frequency of use and amount eaten were the primary issues. Dietary changes were tailored to each child’s individual needs and desires and usually only one change was made in the diet at a time,

The evaluation of compliance to diet in a cohort of free-living subjects is difficult. Compliance was evaluated in several ways: 5-day diet diaries were completed by the patient and parents at the time of admission, at 18 weeks, 36 weeks, 52 weeks, and every 6 months thereafter following admission; these diaries were reviewed by the dietitian and the entries were reviewed with the patient and parents. Worksheets were completed by the patient and parents

every 6 weeks to assess the patients’ and parents’ understanding of the nutritional recommendations; these were discussed in

meet-ings of the dietitian and family. We believe compliance was

ac-ceptable for the purposes of the study.

RESULTS

Table 2 presents descriptive statistics for initial values of the dietary and serum variables. At the time

TABLE 2. Admission Evaluation

fat Saturated fat, g

% Calories from sat-urated fat Polyunsaturated fat,

g

% Calories from pol-yunsaturated fat Dietary cholesterol,

mg/d

Serum variables, mg/ dL

Total cholesterol LDLt cholesterol HDL cholesterol Triglycerides

* Coefficient of variation = standard deviation/mean.

t Low-density lipoprotein.

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of admission, the average of the daily mean total

calories was 1475.5; the average of the daily mean

percentage of calories from total fat was 29.4%; from

saturated fat, 9.0%, and from polyunsaturated fat,

4.2%. The mean intake of saturated fat was 14.8 g.

The mean daily cholesterol intake was 132.5 mg. The

mean serum total cholesterol level at entry was 201.8

mg/dL; LDL-C, 147.7 mg/dL; HDL-C, 44.8 mg/dL;

and triglycerides, 59.7 mg/dL.

Table 3 summarizes variable values at the times of

the last measurements, and Table 4 shows the

changes in dietary and serum variables (final minus

initial). At the final dietary assessment, the daily mean total calorie intake increased to 1544.3 (not significant [NSJ); the daily mean percentage of calories from total

fat decreased to 29.2 (P .016), and the mean

per-centage of calories from saturated fat decreased to 7.7

(P = <.001). The mean intake of saturated fat

de-TABLE 3. Final Values

Dietary Variables Mean (Range) SD CV* Average calories 1544.31 (892-2706) 417.73 0.27 Total fat, g 49.04 (25-90) 16.58 0.34

%Calories from total 29.22 (19.6-81.1) 10.68 0.37 fat

Saturated fat, g 13.18 (6.2-28.2) 4.99 0.38

% Calories from satu- 7.68(4.7-13.2) 1.95 0.25 rated fat

Polyunsaturated fat, 7.25 (3.0-24.0) 4.16 0.57

g

% Calories from pol- 4.29 (1.7-9.9) 2.06 0.48 yunsaturated fat

Dietary cholesterol, 110.18 (47-214) 33.52 0.30

mg/d

Serum variables, mgi

dL

Total cholesterol 190.88 (149-312) 34.20 0.18 LDLt cholesterol 132.48 (85.7-276.0) 37.54 0.28 HDL cholesterol 45.06 (26-64) 9.02 0.20

Triglycerides 83.38 (28-242) 50.41 0.60

* Coefficient of variation = standard deviation/mean. t Low-density lipoprotein.

High-density lipoprotein.

TABLE 4. Differe nces Between Admission and Fina 1 Evaluation

Dietary Variables Mean (Range) SD P Value*

Average calories 68.84 (-716-1081) 396.09 .430 Total fat, g 0.62 (-49-51) 20.94 .906

% Calories from to- -0.13 (-14.0-53.9) 11.84 .016 tal fat

Saturated fat, g -1.66 (-15.7-9.2) 5.04 .115

% Calories from sat- -1.35 (-5.4-2.1) 1.93 <.001 urated fat

Polyunsaturated fat, 0.51 (-11.5-15.7) 5.75 .570

g

% Calories from pol- 0.05 (-8.8-7.0) 3.43 .546

yunsaturated fat

Dietary cholesterol, -22.28 (-145-109) 64.20 .101 mg/d

Serum variables, mg/dL

Total cholesterol -10.97 (-38-45) 20.99 .003 LDLt cholesterol -15.20 (-41.7-36.8) 18.98 <.001 HDI4 cholesterol 0.25 (-12-24) 6.37 .960 Triglycerides 25.29 (-47-203) 52.10 .034

* P values are for two-sided signed rank tests of whether the

changes are significantly different from zero. t Low-density lipoprotein.

High-density lipoprotein.

creased to 13.2 g (NS). However, these values varied

widely among patients, with final percentage of

cal-ories from total fat ranging from 19.6 to 81 .1, per-centage of calories from saturated fat from 4.7 to 13.2,

and grams of saturated fat from 6.2 to 28.2. The

percentage of calories from polyunsaturated fat

in-creased to an average of 7.25 and dietary cholesterol decreased to an average of 1 10.2 mg; neither of these differences was statistically significant.

Among the lipid measurements, significant

de-creases were observed in LDL-C (mean 132.5 mg/dL,

P < .001) and total serum cholesterol (mean 190.9 mg/dL, P = .003); see Tables 3 and 4. Triglyceride

levels increased significantly (P = .034), to a mean

value of 83.4 mg/dL. There was no significant change

in HDL-C level. The range for final LDL-C

measure-ments was 86 to 276 mg/dL; for HDL-C, 26 to 64

mg/dL; for total cholesterol, 149 to 312 mg/dL; and

for triglycerides, 28 to 242 mg/dL.

Spearman rank correlation coefficients were used

to examine relationships between changes in LDL-C

values and changes in dietary variables (Table 5).

There was a significant correlation between LDL-C

changes and change in grams of dietary saturated fat

(P = .025). There were no significant correlations

between change in LDL-C and changes in total fat,

polyunsaturated fat, and dietary cholesterol. We also

analyzed the rates of change of LDL-C (magnitude of

change divided by time between initial and final

measurements, in milligrams per deciliter per day).

The rate of change of LDL-C was significantly

cone-lated with change in grams of saturated fat (P = .004)

but not with any of the other dietary variables.

The average decrease in LDL-C was 10.4% for the

group. Eighteen of the 32 had at least a 10%

reduc-TABLE 5. Statistical Analysis

Dependent Variable : Change i n LDL (Final - Initial) Independent Variable Pearson P Spearman P

(Change = Final - Ini- Come- Value Cone- Value

hal) lation lation

Total fat, g .261 .148 .275 .128

% Calories from total fat .003 .986 .000 .998

Saturated fat, g .296 .100 .396 .025

% Calories from satu- .015 .936 .014 .938

rated fat

Polyunsaturated fat, g .297 .099 .161 .380

% Calories from polyun- .135 .463 .070 .703

saturated fat

Dietary cholesterol, mg/ .142 .437 .123 .501 d

Dependent Variable: Rate of Change of LDL* (U/d)

Independent Variable

(Change = Final - Ini-tial) Pearson Come-lation P Value Spearman Come-lation P Value

Total fat, g

% Calories from total fat

.164 -.095 .370 .606 .303 .022 .092 .903

Saturated fat, g

% Calories from

satu-.314 .048 .080 .793 .494 .100 .004 .586 rated fat

Polyunsaturated fat, g

%Calories from

polyun-saturated fat .437 .274 .013 .130 .224 .126 .219 .492

Dietary cholesterol, mg/ d

.035 .850 .091 .619

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0

r=0.296 (P-0.1)

I I i I I I I I i#{149} I

20

0)

E ____________________________ _______________

, -20

-15 -10 -5 -3 -2 .1 0 1 2 3 5

I. ReduCtiOn ‘I. Increase ‘I

A Sat. fat, 9

Fig 1. Individual change in grams of dietary saturated fat plotted against change in milligrams per deciliter of calculated low-density lipoprotein (LDL) cholesterol.

C

0

Lu.

0

Change in LDL, %

Fig 2. Frequency of the percentage of decrease or increase in low-density lipoprotein (LDL) cholesterol between first and last lipid measurements.

.40 -30 -20 -10 10 20 30 40

30

0

c O

190 110 150 03

E 130

-I

0 110 -I

90 10

100 2 m 400 500 600

0 100 200 0 400 500 600

Days from entry

22 20 0) 18

i 16

14

c 12

10

220 200

#{149}0 03 180 . 160 140 120 100

Fig 3. Upper panel demonstrates change in grams of dietary satu-rated fat in six individuals and corresponding low-density lipopro-tein (LDL) cholesterol levels in the lower panel (diet “responders”).

0 100 200 4153 500 600 700 800 Days from entry

Fig 4. Upper panel demonstrates change in grams of dietary satu-rated fat in six individuals and corresponding low-density lipopro-tein (LDL) cholesterol levels in the lower panel (diet “nonrespond-em’).

tion. Although there was an overall correlation of

change in the amount of saturated fat in the diet with

change in LDL-C, there was considerable individual

variability in response of LDL-C to change in

satu-rated fat (Figs 1 and 2). Some individuals had large

decreases in LDL-C with decreases in dietary

satu-rated fat, whereas others demonstrated a lesser

de-crease or even an increase of LDL-C with similar

dietary changes. In Fig 3, dietary and LDL-C changes

are demonstrated in six patients in whom there was

an appropriate LDL-C response to change in dietary

saturated fat (responders). In Fig 4, dietary saturated

fat amounts and corresponding LDL-C levels are

demonstrated in six patients who did not have an

appropriate LDL-C response to change in dietary

saturated fat (nonresponders).

DISCUSSION

Interpretation of the data was made difficult

be-cause of certain confounding factors.

All children in this study were referred to the

Health Clinic because they came from families in

which an adult member had hyperlipidemia or

pre-mature cardiovascular disease, and all had LDL-C

levels of 1 1 0 mg/dL or higher. As a result, the cohort

could have been enriched with children in whom the

genetic effect on lipid levels is stronger than in the general population.

In addition, many of the families already had mod-ified the family diet and some of the children at the time of admission were eating diets with total fat less

than 30% of calories and cholesterol less than 300

mg/d. Dietary counseling involved not only decreas-ing total fat, saturated fat, and cholesterol intake in

10 some children, but also increasing dietary fat in five

children in whom dietary total fat calories were less than 20%. The goal of the diet program was a gradual

movement of both groups of children toward a Step

1 Diet. The fact that the initial diet of some of the children was already low in total fat, saturated fat, and cholesterol suggests that the results, after change in diet, may understate results that could occur if the initial diet had been higher in total fat, saturated fat, and cholesterol.

The low (4.2% of calories) dietary polyunsaturated

fat at the time of admission and our inability to

significantly increase this percentage in most children

was surprising. The major reason for this was that

the children in the study used very little

oleomargar-me and preferred to increase their fat intake with

foods high in monosaturated fat such as peanut

but-ter.

Although, for the group as a whole, there was not

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correlated with changes in LDL-C concentration. This correlation did not exist for change in the percentage of total calories provided by saturated fat. This

sug-gests that the actual amount of saturated fat in the

diet and not its contribution to total calories affected LDL-C level.

The results of this study indicate that a short-term reduction of the grams of dietary saturated fat coin-cides with a reduction in serum total cholesterol and

LDL-C values in most children with elevated LDL-C,

without adversely affecting serum HDL-C level and

with only a slight increase in total triglyceride value.

However, there is a marked individual variability in

response of LDL-C.

It has been reported that a maximum reduction of

about 10% to 15% of serum LDL-C can be expected

through dietary modification alone. In this study, 18

of the 32 patients reduced their LDL-C levels by at

least 10% following the initiation of diet modification.

The average reduction was 10.4%, but some children

had large changes in LDL-C level associated with

modest dietary changes, whereas others had only

small changes in LDL-C level. It was recognized that

changes in serum lipid and lipoprotein levels could, in part, be the result of regression to the mean. One

might expect that, if regression to the mean were

operating, those patients with the highest initial levels

of LDL-C would show the largest decreases in

LDL-C

over the course of their involvement in the program.

A simple correlation of change in LDL-C and initial

value of LDL-C is not enough to resolve this question,

however, because of the automatic negative

correla-tions between the change (final minus initial) and the initial value. This “spurious’ correlation, which

con-founds other reported comparisons of changes in

serum lipids and initial values, has hindered our

assessment of the role of regression to the mean in

explaining our results, and the issue remains

unre-solved.

Elevated LDL-C is the result of both environmental (mainly diet) and genetic factors. It is not possible at present to predict, in an individual child with elevated

LDL-C, what the relative effects of environment and

genetics may be in causing the elevation. Those with

marked elevations of LDL-C (>200 mg/dL) are likely to have a monogenic form of hypercholesterolemia

and will respond the least to dietary changes. Most

of the children, however, will have levels between

1 1 0 mg/dL and 1 60 mg/dL and are likely to have a

polygenic form of hypercholesterolemia. It is in this

group that one can expect an average reduction in

LDL-C of 10%; if this reduction were maintained into

adulthood, it would result in about a 20% reduction in the incidence of coronary heart disease. However, it is in this group that response to diet may be most

unpredictable, in spite of dietary compliance. It is

important to monitor lipid levels during dietary man-agement and, as the patient approaches adolescence, if the LDL-C level remains significantly elevated, drug treatment has to be considered.

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1992;89;925

Pediatrics

M. Huse, Paul Murtaugh and William H. Weidman

Eric S. Quivers, David J. Driscoll, Colleen D. Garvey, Ann M. Harris, Jay Harrison, Diane

Low-Density Lipoprotein Cholesterol Levels

Variability in Response to a Low-Fat, Low-Cholesterol Diet in Children with Elevated

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1992;89;925

Pediatrics

M. Huse, Paul Murtaugh and William H. Weidman

Eric S. Quivers, David J. Driscoll, Colleen D. Garvey, Ann M. Harris, Jay Harrison, Diane

Low-Density Lipoprotein Cholesterol Levels

Variability in Response to a Low-Fat, Low-Cholesterol Diet in Children with Elevated

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