Interrelationship of Serum Lipids

Interrelationship of Serum Lipids
with Relative Weight, Blood Glucose,
and Physical Activity
By MARIO R. GARCIA-PALMIERI, M.D., RAU'L COSTAS, JR., M.D.,
JOYCE SCHIFFMAN, M.S., ANGEL A. COL6N, M.D., RAQUEL ToRREs, M.S.,
AND
EMILIO NAZARIO, M.S.
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SUMMARY
Serum cholesterol, serum glyceride, blood glucose, relative weight, physical activity,
percent calories from fat, percent calories from carbohydrate, and polyunsaturated/saturated fatty acid (P/S) ratio were determined in 1780 rural and 4023 urban fasting men
aged 45-64 years being followed prospectively to ascertain reasons for the low prevalence of coronary heart disease mortality in Puerto Rico as compared to other countries.
Lipid and glucose levels and relative weight were higher and physical activity lower in
urban men. Glyceride was positively correlated with cholesterol, glucose, and relative
weight, and negatively correlated with physical activity. Cholesterol was positively
correlated with glyceride, glucose, and relative weight, and not correlated with
physical activity. Percent calories from fat and P/S ratio were significantly higher
and percent carbohydrates from starch significantly lower in urban men. These variables taken together were not significant in predicting the differences between urban
and rural serum cholesterol or glyceride values. Relative weight was the most significant
variable in explaining urban-rural differences in serum glyceride and cholesterol levels.
These findings confirm the importance of weight control in dietary management for
reduction of serum lipids.
Additional Indexing Wordt
Coronary heart disease
Urban-rural comparisons
Physical activity
Diet
Relative weight
the figures for age-specific death rates in 1963
were very low when compared to other
countries, particularly the United States.'
An epidemiologic prospective study has
been in progress in Puerto Rico since 1965 in
an effort to explain the low CHD mortality by
studying the influence of so-called risk factors
on the development of the disease. Urban and
rural males are included in a 2:1 proportion,
as preliminary investigations conducted in
1964 had shown statistically significant urbanrural differences in several characteristics
claimed to be related to the development,of
CHD.2 3
The present study of 9814 males has
confirmed substantial urban-rural differences
in monthly income, frequency and intensity of
HEART DISEASE is the most common
cause of death in Puerto Rico, and
among its forms coronary heart disease
(CHD) is the most frequent. In spite of this,
From the Department of Medicine of the School of
Medicine of the University of Puerto Rico, San Juan,
Puerto Rico.
Supported by Contract P.H. 43-63-620 of the
National Heart and Lung Institute, U. S. Public
Health Service.
Presented at the 43rd Scientific Sessions of the
American Heart Association, Atlantic City, New
Jersey, November 13, 1970.
Address for reprints: Dr. Mario R. Carcla-Palmieri,
Department of Medidine, University of Puerto Rico
School of Medicine, San Juan, Puerto Rico 00905.
Received January 18, 1971; revision accepted for
publication November 29, 1971.
Circulation, Volume XLV, April 1972
Serum lipids
Blood glucose
829
830
smoking, physical activity, relative weight,
vital capacity, systolic and diastolic blood
pressure, heart rate, nutrients, blood glucose,
serum cholesterol and glycerides, and prevalence of diabetes and hypertension.4 In view
of these findings it seemed proper to explore
the possible interrelationships of serum cholesterol and glyceride levels with relative weight,
blood glucose, and physical activity. The
purpose of this paper is to present these
relationships.
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Material and Methods
The study includes 2976 rural and 6838 urban
men for a total of 9814, which represents 80.7% of
subjects receiving an appointment after a houseto-house census was conducted in the study
areas.
The details of each study performed and of the
specific laboratory procedures utilized have been
reported elsewhere.5-12 Serum cholesterol was
determined by a modified Huang method,'3
glycerides by the method of Van Handel and
Zilversmit,14 and blood glucose by the NelsonSomogyi method.'.)- Dietary information was
obtained by the 24-hour recall technic.16 The
physical activity index represents the sum of the
products of weighted hours spent in five specified
degrees of activity, i.e., none, sedentary, light,
moderate, and heavy. 17 Relative weight, expressed as percent of ideal weight, is the ratio of
the observed weight to the ideal weight for the
observed height multiplied by 100.
Tables are presented showing means, standard
deviations, and mean differences between the
urban and rural values for the variables under
investigation. It should be noted that a significant
difference in a variable between the urban and
rural populations does not indicate that this
variable accounts for a corresponding difference
in lipid values. For example, if blood glucose and
serum cholesterol are significantly lower in the
rural than in the urban population, it does not
follow that blood glucose levels are related to
serum cholesterol levels. Simple correlation coefficients between lipid levels (fasting glyceride and
serum cholesterol) and the variables relative
weight, blood glucose, and physical activity index
are also presented for the urban and rural
populations. This coefficient gives a measure of
how closely the variables are related to each other
within the urban and rural populations separately.
Multiple regression equations were generated
for both the urban and rural populations to
answer the question, "How much of the difference
in fasting glyceride (or serum cholesterol) values
GARCIA-PALMIERI ET AL.
between urban and rural populations can be
explained by differences in relative weight, blood
glucose, and physical activity index?"
The urban regression equation fitted by the
least-square method is:
Yill - a,, +bl, X ill, + b2,1, X i2ii + b3,n Xij3, + ei,,
where Yi,, is the dependent variable (fasting
glyceride or serum cholesterol) observed for the
ill, urban subject, a,, is the intercept for the
urban population, XI,,, is the relative weight of
the it"l urban subject, Xl,, is the blood glucose of
the it" urban subject, XiS3, is the physical activity
index of the it"1 urban subject, b1,l is the multiple
regression coefficient of relative weight, b21, is the
multiple regression coefficient of blood glucose,
b:3,, is the multiple regression coefficient of the
physical activity index, and el,, is the error term
for each urban subject.
The rural equation:
Yir= ar + bll. Xii, + b.,r Xj2r + b3r Xi3i. + ei,.
was fitted as above using the values of the rural
rather than the urban subjects.
In order to estimate the urban-rural differences
in lipid values when differences in the three
independent variables are taken into account the
following method was used. The means of the
rural independent variables relative weight, blood
glucose, and physical activity index were
"plugged" into the urban regression equation.
This gives a predicted glyceride (or serum
cholesterol) value based on the rural values for
the three independent values. By inserting the
urban means for the independent variables into
the rural regression equation a predicted triglyceride (or serum cholesterol) value for the urban
population is obtained. Subtracting these two
predicted values gives a predicted urban-rural
mean difference in lipid values based on
differences in relative weight, blood glucose, and
physical activity index.
The above method was also applied using three
diet variables as independent variables.
Results
Although subjects were asked to come in
fasting, only 1780 rural and 4023 urban men
aged 40-69 years did so, for a total of 5803
subjects (table 1). Only fasting subjects were
analyzed to insure postabsorptive levels of
serum glyceride. Table 2 presents mean values
of the variables under study. The rural values
are age-adjusted to the age distribution of the
urban group. Serum glyceride, cholesterol,
blood glucose levels, and relative weight were
Circulation, Volume XLV, April 1972
SERUM LIPIDS AND OTHER VARIABLES
831
significantly higher in the urban group. The
physical activity index, on the other hand, was
significantly higher in the rural men. These
differences in serum glyceride, cholesterol,
blood glucose, relative weight, and physical
Table
activity index were significant at the 1% level
for each age group studied.
Glyceride values were significantly higher
in younger than older subjects among urban
males, but no striking age trend was found in
the rural group (table 3). This finding should
not be interpreted to mean that triglyceride
values tend to decrease as a subject gets older,
but simply that there is a difference between
younger and older urban males in the
examined cohort. The trend of cholesterol was
similar although not as obvious.
Hyperglyceridemia (160 mg/ 100 ml and
over), hypercholesterolemia (250 mg/100 ml
and over), hyperglycemia (110 mg/ 100 ml
and over), and obesity (relative weight 120%
1
Distribution of 5803 Fasting Males by Area of
Residence and Age
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Age
(yr)
Rural
Urban
40-49
50-59
60-69
Total
387
898
493
1780
1089
1989
943
4023
Table 2
Mean and Standard Deviation of Specific Variables in Fasting Males Aged 40-69 Years
by Area of Residence
Variable
Mean
SD
Mean
SD
Difference*
minus
~~~~~~~(urban
rural)
Glycerides (mg/lOOml)
127
193
93
104
38
74
39
24
16
10
160
206
98
117
127
33
42
32
11
5
19
6
13
7
Rural
Rural
Cholesterol (mg/100 ml)
Glucose (mg/100 ml)
Rtelative weight (%)
Physical activity index (units)
Urban
31
*Significant at 0.01 level.
Table 3
Mean and Standard Deviation of Serum Cholesterol and Glycerides by Age in Urban
and Rural Fasting Males
Cholesterol (mg/100 ml)
Rural
Glycerides (mg/100 ml)
Age
(yr)
Mean
SD
Mean
SD
Mean
SD
40-49
50-59
60-69
Total
194
197
193
195
40
38
40
39
208
206
39
43
71
74
202
206
42
42
129
127
125
127
Urban
Rural
74
74
Urban
Mean
SD
173
138
161
141
160
136
84
127
Table 4
Males Aged 40-69 Years with High Levels of Specific Variables
Variable
Glycerides > 160 mg/100 ml
Cholesterol > 250 mg/100 ml
Glucose > 110 mg/100 ml
Relative weight > 120%
Circulation, Volume XLV, April 1972
Rural males
Urban males
(%)
P
19
8
7
17
33
<0.01
<0.01
<0.01
<0.01
(%)
14
12
45
GARCiA-PALMIERI ET AL.
832
Table 5
Correlation Matrix of Serumn Cholesterol and Glycerides with Other Variables
Serum
cholesterol
Triglyceride
Variable
Triglyceride
Serum cholesterol
Relative weight
Glucose
Physical activitv
1.00
Triglyceride
Seruim cholesterol
Relative weight
Glucose
Physical activity
1.00
Rural
0.4.5
1.00
Relative
weight
Glucose
Physical
activity
0.35
0.22
1.00
0.19
0.13
0.18
1()
-0.11
-0.02
-0.08
-0.07
1.00
0.20
0.13
1.00
0.17
0.09
0.12
1.0
-0.07
-0.01
-0.06
-0.06
1.00
Ur ban
0.39
1.00
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Table 6
Actual and Predicted Differences in Mea.n Cholesterol and Glycerides between 3988 Urban and
1763 Rural Males
Age (yr)
40-49
5)0 -59
60-69
Total
Difference (urban minus rural)
Cholesterol (mg/100 ml) Glycerides (mg/100 ml)
Actual
Actual
Predicted*
Predicted*
15
10
1(0
12
81
23
5
45
32
1.)
6
31
20
7
.5
*FL.on variables: relative weight, blood
physical activity iiidex.
7
gltueose,
aiid
and over) occurred about twice as frequently
in the urban area, and the differences were
statistically significant (table 4).
Serum glyceride was positively correlated
with serum cholesterol, blood glucose, and
relative weight, and negatively correlated with
physical activity. Serum cholesterol was positively correlated with serum glycerides, blood
glucose, and relative weight, and not correlated with physical activity (table 5).
Table 6 shows urban-rural differences in
serum cholesterol and in serum glycerides, as
well as the differences which would be
predicted by multiple regression analysis on
the basis of urban-rural differences in relative
weight, blood glucose, and physical activity
index. Of the three variables analyzed the one
that was most significant in predicting the
differences between urban and rural serum
glyceride values was relative weight; blood
glucose was next; and physical activity was
least significant. The situation with cholesterol
was somewhat different. Relative weight was
the most significant variable in explaining
differences in cholesterol level in all age
groups; blood glucose was also significant,
except in the rural age group 60 to 69 years;
but physical activity index was not significant.
Table 7 presents urban and rural differences
in several diet variables. These computations
excluded subjects who reported unusual dietary intake due to illness, etc. There is a
significant difference in all these variables.
However, table 8 shows that there is a low
correlation between these variables and both
glyceride and serum cholesterol values. It
should be noted that the small correlations
reported here between diet variables and lipid
levels could be due to the large measurement
error inherent in diet measurements based on
a 24-hour recall. If there is any real correlation
this measurement error will tend to understate
it. However, Balogh et al.18 who administered
repeated 24-hour recall histories, did not find
any evidence that the correlations between the
diet variables and serum cholesterol approached larger values with these more
precise estimates. Thus the possibility remains
that the correlation between diet and lipid is,
in fact, low and is not due to the excessive
measurement error.
Circulation, Volume XLV, April 1972
833
SERUM LIPIDS AND OTHER VARIABLES
Table 7
Mean and Standard Deviation of Diet Variables in Fasting Males by Area of Residence
Mean
SD
Mean
SD
Difference*
(urban minus rural)
32
0.3.5
7
0.30
37
0.54
8
0.47
.
0.19
71
2373
11
35
14
847
9
18
16
308
41
34
107
3
9
62
2436
17
39
37
433
102
89
278
14.8
46
16
828
13
19
17
31 5
43
.34
104
3
9
-9
61
6
4
3
Urban
Rural
Diet variable
% calories from fat
P/S ratio
% carbohydrate from
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starch
Calories
PFA
MFA
SFA
Cholesterol
Total fat
Total protein
Total carbohydrate
calories from protelln
Cc calories from
carbohydrate
/
34
368
87
8.5
302
14.3
52
85
13
4
-24
0.3
-6
*Significant at 0.01 level.
Abbreviations: P/S ratio - polyunsaturated/saturated fatty acid ratio; PFA - polyunsaturated
fatty acids; MFA = monouinsaturated fatty acids; and SFA = saturated fatty acids.
Table 9 shows urban-rural differences in
serum cholesterol and in serum glyceride for
each age group. Also shown are the differenices that would be predicted by multiple
regression analysis for each age group on the
basis of urban-rural differences in percent
calories from fat, P/S ratio, and percent
carbohydrates from starch. Discrepancies in
the tables of reported differences are due to
excluding unknown values and rounding error.
These three diet variables were chosen to give
an indication of the kind and amount of fat
and carbohydrate eaten, which are the most
pertinent factors for inclusion in a brief
analysis. Calories were not included in the
multiple regression because caloric intake
Table 8
Correlation Coefficients of Triglycerides and Serum Cholesterol of Fasting Males with
Diet Variables
Sertum cholesterol
Diet variable
Calories
PFA
MFA
SFA
Cholester.ol
Total fat
Total proteiin
Total carbohydirate
P/S ratio
% carbohydr.ate from starch
% caloiies from fat
( calories from piotein
% calories from carbohydrate
Triglyceride
Urban
Rural
Urban
Rural
0.03
0.03
0.07
0.07
0.08
0.07
0.06
-0.04
-0.01
-0.02
-0.01
-0.01
0.01
-0.01
0.00
(.00
-0.08
-0.03
0.06
0.11
-0.10
0.04
0.06
0.04
0.04
0.04
0.05
-0.06
-0.01
-0.03
-0.07
0.05
0.06
-0.08
0.10
0.08
-0.13
0.01
0.02
0.04
0.01
-0.05
-0.07
-0.04
-0(.01
-0.01
-0.03
0.01
-0.04
(.01
0.03
-0.05
Abbreviations: P/S ratio = polyunsaturated/saturated fatty acid ratio; PFA = polyunsaturated
fatty acids; MFA = monounsaturated fatty acids; and SFA = saturated fatty acids.
Cir-culation, Volume XLV, April 1972
GARCIA-PALMIERI ET AL.
834
Table 9
Actual and Predicted Differences in Mean Cholesterol and Glycerides between 3125 Urban and
1552 Rural Males
Age (yr)
40-49
50(59
60-69
Total
Difference (urban minus rural)
Glycerides (mg/100 ml)
Actual
Predicted*
Cholesterol (mg/100 ml)
Predicted*
Actual
1
14
8
8
10
2
_
1
1
43
29
14
29
3
3
2
1
*Froin diet variables: % calories from fat, polyunsaturated/saturated fatty acid ratio, and % carbohydrates from starch.
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would reflect weight and physical activity,
rather than diet composition. Dietary cholesterol was also excluded, because Puerto Rican
intake is considerably lower than in mainland
United States men. Note from table 8 that the
three diet variables chosen a priori do have
larger correlation coefficients with lipid levels
than most of the other nutrients. The percent
calories from carbohydrates shows one of the
strongest correlations with the lipid values;
however, it was not included in the multiple
regression equation because this variable is
highly correlated with percent calories from
fat. None of these variables in table 9 was
significant in predicting urban-rural difference in either fasting glyceride or serum
cholesterol.
Discussion
The analysis of the data obtained by
comparing 1780 rural and 4023 urban Puerto
Rican fasting males, aged 40-69 years, revealed substantial differences in serum glycerides, serum cholesterol, relative weight, blood
glucose, and physical activity.
In the present study no correlation of
physical activity with serum cholesterol was
found. Contrariwise, Stulb and coauthors have
reported a significant inverse relationship
between exercise and serum cholesterol in 26
pairs of age-matched white men in Evans
County, Georgia.19 This seeming contradiction
might be explained on the basis of the
differences in the methodology utilized to
measure physical activity and in the size and
method of selection of the samples studied.
As much as half of the difference in serum
cholesterol between urban and rural populatioils, and as much as two thirds of the
differenice in serum glycerides, could be
explained on basis of differences in relative
weight, blood glucose, and physical activity
index. Of these variables, relative weight was
the most significant determin-ant of both
glyceride and cholesterol levels.
In the Framingham study20 it was found
that "generally speaking, both weight and
weight change appear to have a weak
association with serum cholesterol level." A
study conducted on 104 psychiatric patients21
to evaluate the relationship of obesity to
triglycerides, cholesterol, glucose, and uric
acid revealed significant independent relationship of obesity to serum glycerides and that
"iin spite of the overall high total relationship
between the four biochemical measures and
obesity, serum cholesterol was found to
contribute little to the total correlation." In
another study on 240 veterans admitted to the
hospital, on the other hand, a significant
relationship between serum cholesterol and
body weight was found.22
The urban-rural differences in serum cholesterol and glycerides could not be explained by
the predicted differences that would be
expected from the three diet variables. This
finding of a lack of relationship of these three
dietary elements with serum cholesterol in
free-living individuals is in agreement with the
previously reported lack of relationship of
different nutrients to serum cholesterol levels
in population studies.'9' 20. 23. 24 The present
analysis does not suggest that change in an
individual's diet does not influence his glyceride or serum cholesterol values. All that cain be
said is that differences in diet found in this
free-living population do not account for
differences in their lipid levels.
On basis of animal experiments, clinical
investigations, and prospective epidemiologic
studies, there has accumulated substantial
evidence to link serum lipids, especially
cholesterol, with the development of atherosclerosis and coronary heart disease. This has
Circulation, Voluine XLV. April 1972
835
SERUM LIPIDS AND OTHER VARIABLES
awakened considerable interest in the development of measures to alter serum cholesterol
levels. The use of dietary intervention as a
possible tool for reducing serum lipids and
preventing the possible development of coronary heart disease is a subject of extreme
importance to many organizations, laboratories, clinics, and physicians today. The
present observations suggest the possibility
that in order to reduce serum lipids by dietary
management weight control should be attained.
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Acknowledgment
We are specially indebted to Dr. William Zukel,
Associate Director for Clinical Applications of the
National Heart and Lung Institute, and Dr. William
B. Kannel from the Framingham Study for their
supervision and continuous advice, without which the
Puerto Rico Heart Health Program could not have
been accomplished. We also thank Dr. William B.
Kannel for suggesting the analysis of these data and
for reviewing the manuscript. The review of the
manuscript by the staff of the Division of Epidemiology and Biometrics of the National Heart and Lung
Institute is also acknowledged.
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Circulation, Volume XLV, April 1972
Interrelationship of Serum Lipids with Relative Weight, Blood Glucose, and
Physical Activity
MARIO R. GARCÍA-PALMIERI, RAÚL COSTAS, JR., JOYCE SCHIFFMAN,
ANGEL A. COLÓN, RAQUEL TORRES and EMILIO NAZARIO
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Circulation. 1972;45:829-836
doi: 10.1161/01.CIR.45.4.829
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