1077
Relations of Body Habitus, Fitness Level, and
Cardiovascular Risk Factors Including
Lipoproteins and Apolipoproteins in a Rural
and Urban Costa Rican Population
Hannia Campos, Stephen M. Bailey, Lisa S. Gussak,
Xinia Siles, Jose M. Ordovas, and Ernst J. Schaefer
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Increased general and abdominal obesity has been independently associated with diabetes,
increased risk of stroke, and coronary artery disease (CAD). It is more prevalent in developed
countries and in urban areas of nonindustrialized nations than in less developed and rural
areas. To evaluate the associations between general and abdominal obesity (as determined by
total body fat, waist to hip ratio, umbilical to triceps ratio, and umbilical to subscapular ratio)
with glucose, plasma lipoproteins, apolipoprotein (apo) A-I and B concentrations, and low
density lipoprotein (LDL) particle size (LDL 1-7), we randomly selected 222 men and 243
women from rural and urban areas of Puriscal, Costa Rica. Abdominal obesity, as assessed by
the waist to hip ratio, was independently and significantly associated with higher triglyceride
levels (p<0.01) and with lower high density lipoprotein cholesterol levels (p<0.05) in men and
women and with higher glucose levels (/?<0.05) and smaller LDL particle size (p<0.01) in
women. Abdominal obesity, as assessed by the umbilical to subscapular ratio, was independently and significantly associated with higher total cholesterol (p<0.005) and apo B (p<0.01)
levels. Umbilical to triceps ratio was positively associated with blood pressure in men. Urban
men had increased general and abdominal obesity (/><0.0001), number of cigarettes smoked
per day (p<0.0001), and diastolic blood pressure (p<0.05) and had a decreased fitness level
(p<0.0001) as well as higher (/?<0.05) plasma glucose, triglyceride, and total cholesterol
concentrations and lower (p<0.05) apo A-I and HDL cholesterol levels compared with rural
men. The differences between rural and urban women were not as striking. Urban women had
increased general and abdominal obesity, glucose, and apo B levels (/?<0.05) and a decreased
fitness level (/><0.0001). Our data indicate that general and abdominal obesity, increased
cigarette smoking, diastolic blood pressure, and decreased fitness level are more prevalent in
an urban than in a rural area in Costa Rica, particularly in men. The higher prevalence of such
risk factors in the urban area is associated with a more atherogenic plasma lipoprotein profile.
(Arteriosclerosis and Thrombosis 1991;ll:1077-1088)
G
eneral and abdominal obesity has been independently associated with increased levels
of cardiovascular disease (CVD) risk factors and mortality and with increased death rates for
all causes. 1 - 5 Although the prevalence of CVD risk
factors is lower in developing countries than in
industrialized nations, 6 the incidence of mortality
From the Lipid Metabolism Laboratory (H.C., L.S.G., J.M.O.,
E.J.S.), US Department of Agriculture Human Nutrition Research Center on Aging at Tufts University, Boston, Mass.; the
Department of Sociology and Anthropology (S.M.B.), Tufts University, Medford, Mass.; and el Institute de Investigaciones en
Salud (X.S.), Universidad de Costa Rica, San Pedro, Costa Rica.
Supported by contract 53-3K06-5-10 from the US Department
of Agriculture. This research was conducted as part of H.C.'s dis-
due to CVD and other degenerative diseases has
increased considerably with industrialization, particularly in urban areas. 6 " 10 An increased prevalence of
obesity, especially abdominal obesity, has been reported to go hand in hand with changes from traditional (rural) to modern (urban) lifestyles.11"14
It has been suggested that in addition to body mass
index (BMI), body fat distribution indicators should
sertation at Tufts University School of Nutrition.
Address for correspondence: Hannia Campos, PhD, University
of California, Donner 265, Berkeley, CA 94720.
Address for reprints: Ernst J. Schaefer, MD, Lipid Metabolism
Laboratory, USDA Human Nutrition Research Center on Aging
at Tufts University, 711 Washington Street, Boston, MA 02111.
Received November 13, 1991; revision accepted April 19, 1991.
1078
Arteriosclerosis and Thrombosis Vol 11, No 4 July/August 1991
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be considered as a measure that may relate to an
atherogenic lipid profile in both men and women.15-16
However, population differences exist in the incidence of abdominal obesity1116"20 and lipoprotein
levels,21-22 and this raises questions as to how different populations will respond to increased abdominal
obesity in the presence of other CVD risk factors.
Results from the European Fat Distribution Study
suggested that the relations of body fat distribution
with serum lipids differed in the five female populations studied.23 Haffner et al16 also reported that
alterations in levels of body fat distribution indicators
could in part account for ethnic differences in high
density lipoprotein (HDL) cholesterol and triglyceride levels between Mexican-Americans and Anglos.16
Adipose tissue distribution patterns have usually
been assessed by several anthropometric indicators
such as the waist to hip ratio (WHR)24-25 and several
upper-body to lower-body or central to peripheral
body contrasts by skinfold measurements at specific
anatomic locations.26"28 Several studies suggest that
an elevated WHR is associated with higher triglyceride23,24,29,3o a n c j total cholesterol concentrations30 and
lower HDL cholesterol levels.2324'29-30 Abdominal obesity has also been associated with increased glucose
and insulin levels2831 as well as with increased prevalence of diabetes27-3233 and higher systolic and diastolic blood pressures, as noted in some34"36 but not
all23 studies. Abdominal obesity, as assessed by the
ratios of several skinfold measurements, has also been
associated with serum lipid levels.23-37-38 A subscapular
to triceps ratio (STR) has been associated with higher
triglyceride and total cholesterol levels as well as with
lower HDL cholesterol levels.23-37-38
It also has been suggested that apolipoproteins
(apos) A-I and B may serve as better predictors of
the presence of coronary artery disease (CAD) than
does HDL cholesterol or low density lipoprotein
(LDL) cholesterol alone.39-40 Apo A-I is a major
protein constituent of HDL, while apo B is a major
constituent of very low density lipoproteins (VLDLs)
and is the sole protein constituent of LDL.41-42 In
addition, heterogeneous groups of LDL with respect
to size and density have also been identified,43 and
small LDL particles have been found more frequently in men and in patients with CAD.44"46 An
elevated WHR has been associated with increased
apo B levels in men and women30 and with decreased
apo A-I levels in postmenopausal women.47 Furthermore, significant associations between body fat distribution and lipoprotein subfractions have been
reported in men and women,38-48 in whom WHR was
negatively correlated with HDL2 and positively with
small LDL and VLDL mass, while the STR was
negatively correlated with large LDL and with VLDL
mass.38
In the present study we have examined the relation
of general and abdominal obesity, fitness level, and
smoking habits with blood pressure, plasma glucose,
lipids, apolipoproteins, and LDL particle size in men
and women from the rural and urban areas of
Puriscal, Costa Rica. Our main objectives were to
test whether CVD risk factors differ between a rural
and an urban non-Anglo population and to examine,
in this population, which abdominal obesity indicators are associated with a more atherogenic plasma
lipid profile in the presence of other established
CVD risk factors.
Methods
Study Population
The study sample was randomly selected from the
canton (county) of Puriscal, Costa Rica. The Puriscal
region extends from the middle of Costa Rica to the
Pacific coast area and comprises about 800 km2.
There are about 26,000 inhabitants in approximately
150 localities of very sparsely distributed rural population, with fewer than 500 people in each locality.
Santiago, while not a true urban center, is the
canton's capital and is the only district in Puriscal
with a centralized population of about 8,000 people.
Moreover, Santiago is referred to as urban by the
Center of Census and Statistics in Costa Rica, and
their definition and maps were used in this study.
This region is rapidly undergoing modernization;
approximately 70% of the homes in the rural area
and 100% in Santiago have access to electricity and a
piped water supply. The rural population subsists
mainly on agricultural products and the sale of food
crops, while professional careers, retail business, and
white-collar jobs predominate in Santiago. The population is predominantly mestizo (mixture of Spanish
and Indian ethnic groups), with a small proportion of
mulattoes (mixture of black and Spanish ethnic
groups). Modern anthropological research suggests
that in Costa Rica a tripartite racial mixing took
place before the 1800s, accompanied by the development of a European way of life.49 Since that time a
comparatively homogeneous Hispanic-American society has formed.50
Stratified random sampling was performed in the
rural and urban areas to obtain a similar number of
participants in each group. Eligible households were
defined as those having one man and one nonpregnant woman aged 20-65 years in 130 households
randomly selected from the 3,415 identified houses in
the rural area and 130 households randomly selected
from the 918 identified houses in the urban area.
Participation rates were 85% (n=222) for men and
93% («=243) for women in both rural and urban
areas.
Subjects with triglyceride levels greater than 400
mg/dl (ra=ll), glucose levels greater than 140 mg/dl
(n=9), positive history of heart disease («=4), taking
medications known to affect lipid levels (n=26),
taking oral contraceptives (n=41), or missing plasma
samples (n=l) were not included in this analysis. The
final sample size was 202 men and 174 women.
Data Collection
Data were collected from January through September 1988. Trained fieldworkers visited partici-
Campos et al Body Fat Distribution, Fitness Level, and CV Risk Factors
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pants in their households for recruitment, where
subjects signed a consent form, and subsequent appointments were made for data collection. A health
history and general characteristics questionnaire was
completed for each subject. The questionnaire included socioeconomic and demographic characteristics as well as a brief medical history, family history of
heart disease, diabetes, hypertension, smoking habits, and physical activity patterns.
Anthropometric measurements. All anthropometric
measurements were taken by three trained fieldworkers who were acquainted with standardized
methods, with subjects wearing light clothing but not
shoes. All measurements were performed in duplicate and were averaged for analyses. Waist (smallest
horizontal trunk circumference) and hip (largest
horizontal circumference around the hip and buttocks) girths were measured with nonstretching fiberglas or metal tapes. Measured skinfold thicknesses
included the triceps (posterior upper arm, midway
between the elbow and acromion), subscapular (1 cm
below the lower tip of the scapula), umbilical (2 cm to
the right of the navel), suprailiac (at the midline and
above the iliac crest), and medial calf. All measurements were taken on the right side of the body with
the use of Holtain skinfold calipers. For this analysis
the abdominal obesity indicators used were WHR,
umbilical to triceps ratio (UTR), and umbilical to
subscapular ratio (USBR). Height and sitting height
were measured by use of a steel anthropometer. To
ensure correct readings to the nearest 0.1 cm for
heights, subjects always stood on a flat surface
against a wall. Weight was determined by use of
either a Detecto bathroom scale or a Seca Alpha
Model 770 digital scale accurate to 50 g. Both scales
were calibrated biweekly. BMI was calculated as
weight in kilograms divided by height in meters
squared. Metropolitan relative weight (MRW) was
calculated as the ratio of observed weight to published values for desirable weight, with use of the
midpoint of the weight range for individuals of
medium frame.51 Individuals were considered obese
if their MRW exceeded 130%. Subjects with an
MRW less than 90% were also identified. Because it
has been suggested that BMI should be used to
determine obesity in cross-cultural comparisons,52 we
calculated that the corresponding BMI cutoff point
for an MRW greater than 130% was at least 27.6
kg/m2 and for an MRW less than 90% was not more
than 20.0 kg/m2 for men and women. BMI was highly
correlated with MRW (r=0.997).
Bioelectric impedance assessment (BIA). All bioelectric impedance measurements were performed
during the morning, before any strenuous activity,
and after a 12-hour fast with a bioelectric impedance
analyzer (model 101, BIA Systems, Detroit, Mich.),
following the procedures previously described by
Lukaski et al.53 Four gel electrodes were attached to
the anterior surfaces of the foot and ankle and to the
posterior surfaces of the arm and wrist. Subjects were
supine on a flat surface, with the arms relaxed at the
1079
sides, not touching the body, and with the thighs
separated. Resistance and reactance were read directly from the instrument. Resistance (R), reactance
(X), and impedance [(R2+X2)1/2] values were measured directly on a subsample of 50 men and 44
women. To estimate total body fat in this subsample
we used the equation developed by Khaled et al,54
where total body fat=impedance x weight/height2.
Lean body mass was then calculated as weight minus
total body fat. In addition, total body fat for the
whole population was calculated by deriving an equation by use of a Max R stepwise multiple regression
procedure, with total body fat as the dependent
variable and several anthropometric measurements
available for the whole population as the independent variables. Significant (p<0.05) anthropometric
measurements were used in the following equations:
For men
Body fat (kg)=21.86-(weightx0.0982)+(BMIx
0.3469)-(sitting height/height x 28.77)+(log triceps
x0.8936)+(umbilicalx0.0647)R2=0.6599
and for women
Body fat (kg)=22.40-(heightx0.1129)+(hipx
0.1643) - (wrist x 0.7793)+(log triceps x 1.7340)
- (umbilical x 0.0501)+(suprailiac x 0.0711)R2
=0.8388
Fitness score. To determine the level of fitness, a
modified Harvard step test was performed on a portable wooden 40-cm step. Subjects were instructed to
step up and down while following the beats of a
metronome. Women were asked to maintain a rhythm
of 76 beats/min, whereas men were asked to follow a
rhythm of 96 beats/min. Subjects were requested to
perform the test for 3 minutes, but when this was not
possible the time during which the exercise was performed was recorded. Pulse rates were taken immediately after the test and at 1 and 3 minutes after the
test. Fitness score (FS) was calculated as seconds
during exercise divided by (pulsel+2+3) times 100.
Blood samples and blood pressure. Blood samples
were drawn into tubes containing 0.1% EDTA after
a 12-14-hour fast. A drop of blood was immediately
obtained from the tube for glucose analysis by an
Accu-Check II Blood Glucose Monitor with Chemstrip bG Test Strips (Boehringer Mannheim Diagnostics, Indianapolis, Ind.) and standardized against
an enzymatic (glucose oxidase-peroxidase) method.
Blood tubes were then immediately stored at 4°C.
Within 36 hours they were centrifuged at 2,500 rpm
for 20 minutes at 4°C to isolate the plasma. HDL
supernates were then obtained after precipitation of
apo B-containing particles with dextran sulfateMg2+ by use of the method of Warnick et al.55 All
1080
Arteriosclerosis and Thrombosis Vol 11, No 4 July/August 1991
plasma aliquots were then stored at — 70cC until they
were transported to the Human Nutrition Research
Center on Aging at Tufts University in Boston where
all the plasma samples were evaluated. Blood pressure was always measured in the morning while the
subject was in a sitting position. All measurements
were taken in duplicate by the same registered nurse
using a sphygmomanometer. The average of the two
measurements was used for this analysis.
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Lipoprotein Analyses
Plasma cholesterol, triglyceride, and HDL cholesterol levels were measured with an Abbott Diagnostics ABA-200 bichromatic analyzer and Abbott
A-Gent enzymatic reagents.56 VLDL and LDL cholesterol levels were estimated for all subjects with
triglyceride levels less than 400 mg/dl by use of the
Friedewald equation.57 Total cholesterol, triglyceride, and HDL cholesterol assays were standardized
through the Centers for Disease Control Lipid Standardization Program, Atlanta, Ga.
Plasma apo B quantification was performed by use
of noncompetitive enzyme-linked immunosorbent assays as previously described.58 This method employs
a double-sandwich technique in which the microtiter
plates (Nunc Immunoplate I, Roskilde, Denmark)
were coated with affinity-purified polyclonal antibody
for apo B. The same methodology was used for
quantification of apo A-I except that affinity-purified
apo A-I antibody and plasma dilutions of 1:60,000
were used. Standards for these assays were calibrated
with reference material obtained from the Centers
for Disease Control.
Gradient gel electrophoresis on 4.9x82x82-mm
2-16% nondenaturing polyacrylamide gels (PAA
2-16%, Pharmacia, Piscataway, N.J.) was performed
to separate LDL subfractions, as previously described.44 Seven LDL bands (LDL 1-7) have been
identified and classified according to the particle
density determined by sequential ultracentrifugation59 or by gradient gel electrophoresis.44 LDL Is
are the largest LDL particles and are found in the
density range of 1.019-1.033 g/ml, whereas LDL 7s
are the smallest particles and have a buoyant density
range of 1.050-1.063 g/ml. Most subjects usually had
one major band and one or two minor bands. To
account for the minor bands, we assigned each
subject a weighted LDL particle score, for which the
relative area under each band present was multiplied
by the band number. For example, a subject with a
predominant band 3 (75% of area) and a minor LDL
band 4 (25% of area) would have an LDL particle
score of 3.25 or [(3x0.75)+(4x0.25)]. A larger LDL
particle score corresponds to a small LDL particle
size because the largest LDL particles are LDL Is
(score=1.00) and the smallest LDL particles are
LDL 7s (score=7.00).
Statistical Analysis
Differences between rural and urban areas for all
parameters measured were evaluated by t test analy-
sis and are presented as mean±SD. Pearson correlation coefficients were used to determine the significant correlations among the various anthropometric
measurements, FS, smoking habits, blood pressure,
plasma glucose, lipids, lipoproteins, apolipoproteins,
and LDL particle size. The stepwise regression procedure was used to identify independent associations
between the anthropometric variables and glucose,
lipoproteins, and blood pressure. All the analyses
were performed with the SAS software package (SAS
Institute, Cary, N.C.). Because the distribution of
several variables (triglycerides; HDL cholesterol; apo
A-I; triceps, subscapular, and calf skinfolds) was
skewed, logarithmic transformations were performed
for analyses involving these variables. Logarithmic
transformations were also used for the skinfold ratios
UTR and USBR.
Results
General Characteristics for Residents of Rural and
Urban Puriscal
Table 1 shows the mean±SD for anthropometric
characteristics in men and women from rural and
urban Puriscal, Costa Rica. Men from the urban area
were heavier (p<0.05), with significantly (p<0.05)
higher lean body mass, total body fat (/?<0.0001),
waist and hip circumferences, and trunk skinfolds
(subscapular, umbilical, and suprailiac) (p<0.0l).
There were twice as many men with an MRW greater
than 130% in the urban compared with the rural
area. The prevalence of obesity in the urban men
(21%) was lower than that previously reported for
the Framingham men (31%) by similar standards.60
The prevalence of an MRW less than 90% was very
similar between rural and urban men. There were no
significant rural-urban WHR differences in men, but
the UTR and the USBR were significantly (/?<0.0001)
higher in urban men. Elevated diastolic blood pressure,
lower fitness level, and a higher prevalence of smokers
(39% versus 16%) were also found in urban men
compared with rural men (Table 2).
Urban women had significantly higher total body fat
(/><0.005), hip circumference (p<0.05), and elevated
QxO.OOOl) lower-trunk skinfolds (umbilical and suprailiac) than did rural women (Table 1). UTR and
USBR were also significantly (p< 0.005) higher in
urban than in rural women, but no significant WHR
differences were detected. In contrast with men, there
were no significant differences in subscapular skinfold
and waist circumference between rural and urban
women, but urban women had significantly thicker
limb skinfolds (triceps and calf) than did rural women.
Urban women were heavier and had a higher prevalence of obesity (MRW>130%) than did rural
women, but these differences were not statistically
significant. The prevalence of obesity in urban Puriscal
women (35%) was higher than that reported for
Framingham women (19%) by similar standards.60 In
addition, urban women had a significantly (p<0.0001)
Campos et al
Body Fat Distribution, Fitness Level, and CV Risk Factors
1081
TABLE 1. Anthropometric Characteristics for Men and Women in Rural and Urban Puriscal, Costa Rica
Women
Men
Variable
Height (cm)
Weight (kg)
BMI (kg/m2)
Body fat (kg)
Lean mass (kg)
> 130% MRW
<90% MRW
Circumferences
Waist (cm)
Hip (cm)
Skinfolds
Triceps (mm)
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Subscapular (mm)
Umbilical (mm)
Suprailiac (mm)
Calf (mm)
Skinfold ratios
WHR
UTR
USBR
Rural
(n = 103)
164.6±7.3
64.9±12.0
23.8±3.1
11.7±1.1
52.7±11.2
Urban
(«=99)
164.9±6.1
68.3 ±10.6*
25.1±3.7f
12.6±1.4*
55.9±9.8*
11%
2%
21%
82.2±8.9
92.7±6.8
85.2±8.7t
95.7±6.1§
77.3±10.0
95.3±9.7
78.6±8.8
98.1±8.1*
9.5±4.9
14.5±7.8
18.3±9.9
21.8±10.6
7.1 ±4.7
10.3±4.8
18.1±8.6§
28.3±12.6t
27.7±11.9§
8.2+4.6
21.5±8.6
25.6±11.2
26.0±9.9
29.4±9.9
20.2±8.9
23.9±7.7*
28.2±10.3
34.3 ±9.5*
35.9±8.5t
23.3±9.5*
0.89±0.05
2.03 ±0.91
1.30±0.51
0.89±0.06
2.82±1.06f
1.61 ±0.59*
0.81 ±0.04
1.30±0.46
1.09 ±0.38
0.80±0.05
1.52±0.48§
1.34+0.414:
2%
Rural
(*=88)
152.8±6.5
59.3 ±11.3
25.4±4.5
14.7±1.8
43.7±9.5
28%
5%
Urban
(n=86)
152.7+6.2
61.0±10.1
26.1 ±4.0
15.4±1.6§
44.8±9.3
35%
1%
BMI, body mass index; MRW, Metropolitan Relative Weight51 (in this population the correlation between MRW and
BMI was r = 0.997. MRW >130% corresponded to a BMI >27.6 kg/m2, and MRW <90% corresponded to a BMI
<20.0 kg/m2) in both men and women. WHR, waist to hip ratio; UTR, umbilical to triceps ratio; USBR, umbilical to
subscapular ratio.
*p<0.05, tp<0.01, +p<0.0001, §p<0.005.
decreased fitness level than did rural women. No
significant rural-urban differences were found in
blood pressure or smoking habits in women (Table 2).
Glucose and Lipoprotein Parameters in Rural and
Urban Residents of Puriscal
Mean±SD for plasma glucose and lipoprotein
parameters for rural and urban Puriscal residents are
TABLE 2. General Characteristics for Men and Women in Rural
and Urban Puriscal, Costa Rica
Men
Rural
Urban
(n = 103) (n=99)
Variable
Age (yr)
41 ±13 39±12
Fitness score*
60±ll
53±10§
Blood pressure
Systolic (mm Hg)
131±12 134±16
Diastolic (mm Hg) 80±9
83±11$
Cigarettes smoked
0/day (%)t
<10/day (%)
>10/day(%)
Women
Rural
Urban
(n=88)
(«=86)
41 ±13 41±11
36±15§
48±13
126±14
77±9
126±13
77±9
62
23
52
9
92
7
89
6
16
39§
1
5
•Fitness score=duration of exercise in seconds divided by (pulse
1+2+3) times 100.
•(•"Cigarettes smoked" includes exsmokers. Probability value is
given for the x2 analysis.
+p<0.05, §/><0.0001.
shown in Table 3. Urban men had significantly
(p<0.05) higher glucose, triglyceride, and total and
VLDL cholesterol levels and significantly (/><0.05)
lower HDL cholesterol, apo A-I levels, and HDL to
total cholesterol ratio (HDL/TC) than did rural men.
LDL cholesterol and apo B concentrations were also
higher in urban men compared with those of rural
men, but these differences were not significant. No
differences in LDL particle size were found between
rural and urban men. Women from the urban area
had significantly (p<0.05) higher glucose and apo B
concentrations. Urban women also had higher triglyceride, total cholesterol, VLDL cholesterol, and
LDL cholesterol levels as well as larger LDL particles, but these differences were not significant. No
significant differences in HDL cholesterol, apo A-I
concentrations, and HDL/TC were found between
rural and urban women.
Correlations Between Body Habitus, Age, Smoking,
and Fitness Level
Correlations between body habitus, age, smoking
habits, and fitness level are shown in Table 4. In men
increased abdominal fat (WHR, UTR, and USBR)
and decreased fitness level were significantly
(/7<O.O5) associated with BMI, total body fat, and
lean mass. Increased smoking was negatively correlated with BMI and lean mass. In addition, age was
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Arteriosclerosis and Thrombosis
Vol 11, No 4 July/August 1991
TABLE 3. Glucose, Lipids, Lipoproteins, and Apolipoproteins for Men and Women in Rural and Urban Puriscal,
Costa Rica
Women
Men
Variable
Glucose (mg/dl)
Triglyceride (mg/dl)
Total cholesterol (mg/dl)
VLDL cholesterol (mg/dl)
LDL cholesterol (mg/dl)
HDL cholesterol (mg/dl)
Apo A-I (g/1)
Apo B (g/1)
LDL particle score*
HDL/TC
Urban
(n=99)
Rural
(n=103)
83±13
133±63
173±34
27+13
105 ±31
42±9
112±21
108 ±36
3.82 ±0.81
0.25±0.06
Rural
(n=88)
84 ±14
117±57
179±42
23±11
110±34
45±9
116±22
97 ±36
3.44±0.89
0.26±0.08
87±llt
161 ±79*
183±31t
32±16*
lll±30
39±9t
105±20t
115 ±35
3.89+0.97
0.22±0.07*
Urban
(n=86)
88+14t
125±62
189±33
25±12
118+29
46±10
116±21
108±34f
3.30±0.86
0.25 ±0.06
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Values are given as mean±SD.
VLDL, very low density lipoprotein; LDL, low density lipoprotein; HDL, high density lipoprotein; apo, apolipoproteins; TC, total cholesterol; HDL/TC, HDL to total cholesterol ratio.
*LDL particle score is the sum of the relative areas under the LDL bands present in each subject, where the largest
LDL particles are LDL 1 (score=1.00) and the smallest, LDL 7 (score=7.00). See text for details.
tp<0.05, *p<0.01.
significantly (p< 0.0001) associated with WHR in
men. In women increased abdominal fat (WHR only)
was positively (p< 0.0001) associated with BMI and
lean mass. UTR was significantly (/?<0.0001) associated with age in women. USBR was not significantly
correlated with any body mass indicator or age. In
contrast, decreased fitness level was correlated
(/><0.005) with age, BMI, body fat, and lean mass in
women. Smoking in women was significantly correlated with decreased lean mass.
UTR only) and decreased HDL cholesterol levels
(WHR only). In contrast, in women elevated abdominal obesity (UTR and USBR only) was significantly
(p<0.01) associated with elevated total and LDL
cholesterol, whereas WHR was associated (p<0.01)
with elevated triglyceride and glucose levels and
decreased HDL cholesterol levels.
Increased fitness level was significantly associated
with decreased triglyceride and total and LDL cholesterol in men and with decreased glucose levels in
men and women. In men smoking was significantly
(p<0.0l) associated with elevated triglyceride and
decreased HDL levels.
Correlations Between Body Habitus, Fitness Level,
and Smoking With Glucose and Lipids
In men, age, BMI, and body fat were significantly
(/?<0.01) and positively associated with triglyceride,
total and LDL cholesterol, and glucose levels and
negatively associated with HDL cholesterol levels
(Table 5). Similar associations were found in women,
but BMI was not significantly associated with total
and LDL cholesterol. In men elevated abdominal
obesity (WHR, UTR, and USBR) was significantly
(p<0.05) associated with increased triglyceride, total
and LDL cholesterol, and glucose levels (WHR and
Correlations Between Body Habitus, Fitness Level,
and Smoking With Blood Pressure, Apolipoproteins,
and Low Density Lipoprotein Particle Size
Elevated systolic and diastolic blood pressures
were significantly (p< 0.005) associated with increased age, BMI, total body fat, and abdominal fat
(WHR and UTR) and decreased smoking (p<0.05)
in men and women (Table 5). Elevated systolic and
TABLE 4. Pearson Correlation Coefficients Between Body Habitus, Fitness Level, and Smoking Habits in Rural and
Urban Puriscal, Costa Rica
Variable
WHR
UTR
USBR
FS
Smoking
Age
BMI
0.47*
0.00
-0.04
-0.06
0.13
0.60$
0.28*
0.14*
-0.37*
-0.16*
Men (n=202)
Body fat Lean mass
0.54*
0.38*
0.21§
0.45*
0.14*
0.37*
-0.44*
-0.17*
-0.17*
-0.05
FS
Age
-0.24§
-0.29*
-0.22§
0.23§
0.30*
0.11
-0.23§
-0.01
-0.05
Women (n = 174)
Body fat Lean mass
0.44*
0.06
0.31*
-0.03
0.00
-0.04
-0.12
-0.02
-0.09
-0.31* -0.30§
-0.23§
-0.14
-0.15
-0.16*
BMI
FS
-0.04
-0.09
0.04
-0.14
WHR, waist to hip ratio; UTR, umbilical to triceps ratio; USBR, umbilical to subscapular ratio; FS (fitness
score)=duration of exercise in seconds divided by (pulsel + 2+3) times 100; BMI, body mass index;
Smoking=cigarettes smoked per day.
*p<0.05, tp<0.01, *p<0.0001, §p<0.005.
Campos et al Body Fat Distribution, Fitness Level, and CV Risk Factors
1083
TABLE 5. Pearson Correlation Coefficients for Body Habitus, Fitness Level, Smoking, Blood Pressure, and Biochemical Parameters in Rural and Urban Puriscal, Costa Rica
Men (n=202)
Variable
TG
Choi
Age
BMI
Body fat
Ratios
WHR
0.16t
0.48*
0.44$
0.22§
0.29$
0.34$
0.41$
UTR
USBR
0.27$
0.25§
0.24§
Smokingtt
0.20§
0.26$
-0.24§
0.10
Age
BMI
0.49$
0.41$
0.45$
0.12
Body fat
Ratios
WHR
UTR
0.38$
0.21t
FS
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USBR
FS
Smoking
0.18f
-0.23§
HDL
LDL
Diast
0.18f
0.18t
0.27$
0.07
0.33$
0.34$
0.24§
0.28$
0.24§
0.27$
0.38$
0.33$
0.16*
-0.34$
0.17t
-0.12
0.24§
-0.08
0.03
0.28$
0.23§
0.12
0.30$
0.23§
0.15*
-0.40$
0.06
0.22§
0.16*
0.11
-0.24§
-0.09
0.59$
0.40$
0.32$
0.54$
0.42$
-0.16*
0.17*
0.26§
0.26§
0.19t
0.08
0.00
-0.24§
0.22§
0.16*
0.07
-0.04
0.27§
0.13
-0.04
-0.10
-0.08
-0.16*
-0.17*
-0.15*
0.08
-0.17f
Women (n = 174)
0.09
-0.29$
0.33$
0.09
0.17*
-0.03
-0.04
-0.27§
0.00
-0.14
0.21f
0.25§
-0.12
0.03
0.04
-0.04
-0.09
-0.01
0.20f
0.27§
-0.07
-0.01
0.26§
0.15*
Syst
Glucose
-0.06
-0.32$
-0.35$
0.11
-0.25§
-0.14*
0.31$
TG, triglycerides; Choi, total cholesterol; LDL, low density lipoprotein cholesterol; HDL, high density lipoprotein
cholesterol; Syst, Diast, systolic and diastolic blood pressures, respectively; BMI, body mass index; WHR, waist to hip
ratio; UTR, umbilical to triceps ratio; USBR, umbilical to subscapular ratio; FS (fitness score)=duration of exercise in
seconds divided by (pulse 1+2+3) times 100; Smoking=cigarettes smoked per day.
*p<0.05, t/><0.01, $p<0.0001, §/?<0.005.
increased age in women. Smaller LDL particles were
positively associated (p<0.01) with BMI, body fat,
and abdominal fat (WHR) in men and women.
diastolic blood pressures were also associated with
decreased fitness levels in men.
The associations between body habitus, apolipoproteins, and LDL particle size are shown in Table 6.
Elevated apo B levels were significantly (p<0.01)
associated with increased BMI and body fat in men
and women and with increased abdominal fat (WHR,
UTR, and USBR) and decreased fitness level in men
and increased abdominal fat (USBR only) in women.
Apo A-I levels were significantly (p<0.0l) associated
with decreased body fat and smoking in men and with
Independent Associations Between Abdominal Fat,
Blood Pressure, and Plasma Parameters
Table 7 shows the standardized /J coefficients of
the stepwise regression models for significant independent associations between total body fat, abdominal fat, plasma parameters, and blood pressure in
men and women. In men elevated total body fat was
TABLE 6. Pearson Correlation Coefficients for Body Habitus, Fitness Level, Smoking, Apolipoproteins, and Low
Density Lipoprotein Particle Size in Rural and Urban Puriscal, Costa Rica
Men {n=202)
Apo A-I
Women (n = 174)
LDL score
Apo A-I
Apo B
Age
BMI
Body fat
0.12
0.24§
0.07
0.41$
0.17*
-0.07
0.36$
0.45$
0.31$
0.29$
-0.09
0.32$
0.23§
0.01
0.36$
0.20t
0.20t
Ratios
WHR
UTR
-0.13
0.24§
-0.13
0.09
-0.01
USBR
FS*
Smoking
-0.17t
-0.08
-0.10
-0.08
-0.19§
Apo B
0.37$
0.27$
0.23§
-0.24§
0.12
0.07
0.05
-0.03
0.04
-0.03
0.10
0.07
0.14
0.21f
-0.14
-0.04
LDL score
0.23§
0.00
-0.12
0.05
-0.09
Apo, apolipoprotein; LDL, low density lipoprotein; WHR, waist to hip ratio; UTR, umbilical to triceps ratio; USBR,
umbilical to subscapular ratio; FS (fitness score)=duration of exercise in seconds divided by (pulse 1+2+3) times 100.
Smoking=cigarettes smoked per day. For LDL score, see footnote to Table 3.
*/?<0.05, tp<0.01, $p<0.0001, §p<0.005.
1084
Arteriosclerosis and Thrombosis
Vol 11, No 4 July/August 1991
TABLE 7. Stepwise Regression Models for Pressure and Biochemical Parameters in Rural and Urban Pursical, Costa Rica
Biochemical parameters
Variable entered
Men (n=202)
Intercept
Total body fat (kg)
Age (yr)
Smoking
Trig
(mg/dl)
Choi
(mg/dl)
-0.037
0.45*
0.007
0.32*
0.22§
0.27*
HDL
(mg/dl)
0.020
-0.37*
-0.15*
FS
WHR
5.30§
USBR
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WHR
USBR
Total R2
Apo B
(mg/dl)
-0.001
-0.32*
0.15*
-0.20t
-0.23f
-0.008
0.44*
0.21§
0.14*
score
Glucose
(mg/dl)
Blood pressure
Systolic
Diastolic
(mmHg)
(mm Hg)
0.002
0.25§
-0.021
0.21§
-0.114
0.22|
LDL
-0.11
-0.089
0.26*
0.14*
-0.16t
0.32*
0.18
-0.28*
-5.55§
3.21
0.46*
UTR
Total R2
Women (n=174)
Intercept
Total body fat (kg)
Age (yr)
Smoking
Apo A-I
(mg/dl)
0.32
0.20
-0.002
0.24§
0.41*
0.030
0.55*
3.86t
0.30
0.85*
0.30
-0.37*
0.21
0.12
0.29
0.10
0.19
0.10
0.023
-0.048
0.22§
0.31*
-0.030
0.20f
-0.004
0.32*
-0.047
-0.045
0.54*
-0.17*
0.55*
-0.18f
0.31
0.31
0.017
-0.28§
0.21t
0.31*
-6.16*
-4.48t
0.17
0.13
0.63t
0.22
5.03§
3.74*
0.10
0.13
Standardized f} coefficients are given for the variables that met the 0.05 level of significance for entering the model. The variable that did
not meet this criteria for any parameter was area of residence (rural or urban). For LDL score, see footnote to Table 3.
TG, triglycerides; Choi, cholesterol; HDL, high density lipoprotein; apo, apolipoproteins; LDL, low density lipoprotein;
Smoking=cigarettes smoked per day. FS, fitness score=seconds divided by (pulse 1+2+3) times 100. WHR, waist to hip ratio; USBR,
umbilical to subscapular ratio; UTR, umbilical to triceps ratio.
*p<0.05, tp<0.01, *p<0.0005, §p<0.005.
very strongly (/?<0.0001) associated with blood pressure and all the plasma parameters. In men age was
significantly (p<0.05) associated with increased total
cholesterol, apo A-I and B levels, and blood pressure.
In men abdominal fat as determined by WHR was
significantly (p<0.01) associated with increased triglyceride and decreased HDL cholesterol and with
smaller LDL particles, but the latter did not reach
statistical significance (/?<0.06). USBR was significantly (p<0.05) associated with higher total cholesterol levels, and UTR, with lower HDL cholesterol
levels and higher diastolic blood pressure. Smoking
was significantly (p<0.05) associated with elevated
triglyceride and apo B levels and with decreased
(p<0.01) HDL cholesterol and apo A-I levels and
lower (/7<0.05) systolic and diastolic blood pressures. Fitness level was also significantly (p<0.05)
associated with decreased glucose and apo A-I levels
in men.
In women total body fat was significantly
(p< 0.005) associated with elevated triglyceride, apo
B, and glucose levels, decreased HDL cholesterol
levels, and smaller LDL particles. Age was significantly (p<0.01) associated with elevated blood pressure and all the plasma parameters except LDL score
and glucose. Similar to the observations in men,
abdominal fat (WHR) was significantly (p<0.01)
associated with increased triglyceride and decreased
HDL cholesterol levels, as well as with smaller LDL
particles. In addition, in women abdominal fat
(WHR) was significantly (p<0.05) associated with
lower apo A-I and higher glucose levels. Abdominal
fat as determined by USBR was significantly
(/><0.01) associated with higher total cholesterol and
apo B levels in women, but UTR was not associated
with any biochemical parameter or blood pressure in
women.
In sum, two abdominal fat indicators were independently associated with different plasma lipoprotein profiles. Increased WHR was associated with a
pattern of increased triglyceride and glucose levels,
decreased HDL cholesterol and apo A-I levels, and
smaller LDL particles. Increased USBR was associated with higher cholesterol and apo B levels. These
associations were independent of other CVD risk
factors such as age, body fat, smoking, and fitness
level. WHR and USBR were the strongest abdominal
fat correlates for these plasma parameters, with no
other significant abdominal fat indicators in the
model (Table 6). Abdominal fat, as determined by
UTR in men, was the only abdominal fat indicator
associated with blood pressure after adjustment for
body fat. Area of residence was not significantly
associated with abdominal fat or plasma lipoprotein
parameters after regression adjustments for body fat,
age, and fitness level were made.
Discussion
Abdominal obesity has been associated with an
increased risk of stroke and CAD.1-3 In women this
Campos et al Body Fat Distribution, Fitness Level, and CV Risk Factors
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association has remained significant after adjustment
for BMI, age, smoking, serum cholesterol and triglyceride levels, and systolic blood pressure.2 Previous
data also indicate that an elevated WHR is associated with higher triglyceride and glucose levels, lower
HDL cholesterol levels,2324-30 and a decreased HDI^
mass and cholesterol.3848 Our data are consistent
with these findings. In both men and women an
elevated WHR was significantly associated with
higher triglyceride levels and lower HDL cholesterol
levels, while an association with glucose was found in
women only. Peiris et al,61 when comparing different
anthropometric measurements as predictors of metabolic abnormalities, concluded that WHR seemed
to be the most useful indicator in premenopausal
women. Consistent with these findings, in our study
WHR was independently and significantly associated
with elevated triglyceride and glucose levels (in
women) and with decreased HDL cholesterol and
apo A-I levels, with no other significant abdominal
fat indicators in the regression model. However, in
both men and women total body fat usually presented
a more significant association with triglyceride, HDL
cholesterol, and glucose levels than did WHR. An
elevated STR has also been associated with higher
triglyceride and lower HDL cholesterol levels.23-37-38
In our study, an STR was not significantly associated
with any lipoprotein parameter (data not shown)
when other anthropometric indicators were included.
The associations between abdominal obesity and
total cholesterol are more variable. A positive correlation between WHR and total cholesterol has been
previously reported in normal men and women in
some30-38 but not all23-34 studies. These discrepancies
could be attributed to methodological or technical
differences such as choice of skinfold site. However,
the European Fat Distribution Study suggests that
there might be considerable population differences in
the relations found between anthropometric indicators of body fat distribution and lipoprotein parameters.23 Our data indicate that in the present population, USBR was significantly associated with higher
total cholesterol in men and women. We did not find
significant correlations between WHR and total cholesterol when USBR was in the model or after
adjustment for other significant covariates. USBR
and WHR are indicators of abdominal obesity, but a
contrast with the upper body rather than the hip
might be more relevant to an association with total
cholesterol in this population.37 The mechanism
whereby abdominal obesity relates to higher CAD
risk is not clear. It has been reported that body fat is
metabolically heterogeneous,62 with varying lipoprotein lipase activity.63 In addition, abdominal obesity
has been characterized by large adipocytes, which
demonstrate increased insulin resistance and increased free fatty acids released into plasma.6465 An
increased amount of free fatty acids reaching the
liver could in turn be associated with increased
triglyceride production and VLDL secretion.66
1085
It has been suggested that plasma apo A-I and B
concentrations may be better predictors of CAD than
are HDL and LDL cholesterol levels.39-40 Anderson
et al30 reported an independent association between
BMI, WHR, and apo B level.30 In our study apo B
levels in men and women were positively associated
with BMI and particularly with total body fat. After
adjustment for total body fat, fitness level, and age, a
positive significant association between USBR and
apo B levels was found in women. WHR was not
significantly associated with apo B levels in this
population after adjustment for body fat. In postmenopausal women it has been reported that apo A-I
is negatively associated with WHR.61 Our data are
consistent with these previous findings. Elevated
WHR was significantly associated with lower apo A-I
concentrations in women, but we did not find a
significant association in males.
We have previously reported that small LDL particles are associated with male gender and increased
age.44 Small LDL particles have also been associated
with the presence of CAD in men.45-46 It has also
been reported that WHR is positively associated with
small LDL particles and VLDL mass in men.38 In the
present study we found a positive association between LDL particle size and age only in women. In
addition, smaller LDL particles were associated with
higher BMI and total body fat in men and women.
WHR was also independently associated with smaller
LDL particles in women. In men the same was true,
but the association was not statistically significant.
Increased prevalence of general and abdominal
obesity has been associated with changes from traditional (rural) to modern (urban) lifestyles.11"14 Population differences in prevalence of abdominal obesityii.16-20 anc j j 1 0 w j t r e i a tes to an atherogenic lipid
profile have also been reported.16-23 Our data indicate that subjects from the urban area are heavier,
and body composition measurements indicate that
the differences observed in weight are particularly
due to elevated total body fat. This observation is
also confirmed by the differences observed in skinfold measurements, particularly the subscapular, suprailiac, and umbilical sites and by the skinfold
ratios, which were significantly higher in the urban
subjects. It should be noted that no difference in the
WHR was found between rural and urban subjects
despite the significant difference found in total body
fat. The prevalence of obesity in urban Puriscal was
10% lower in men and 16% higher in women than
the prevalence of obesity previously reported for the
Framingham population in the United States.60
A higher prevalence of current smokers was also
found in urban compared with rural men. Smoking
habits were in turn associated with higher triglyceride
and apo B levels, as well as with lower HDL cholesterol and apo A-I concentrations. Our data also
indicate that urban men had higher diastolic blood
pressures than did rural men. It has been reported
that central adiposity is associated with elevated
systolic blood pressure.34"36 Our data suggest a pos-
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Arteriosclerosis and Thrombosis
Vol 11, No 4 July/August 1991
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itive association between UTR and diastolic blood
pressure in men, supporting these previous findings.
However, in this population blood pressure was not
associated with abdominal obesity in women. This
finding in women is consistent with previous observations of the associations between body fat distribution and blood pressure in women from the European Fat Distribution Study 23 but differs from other
previous reports. 34 - 36
It has been suggested that some non-Anglo populations may be genetically predisposed to an increased prevalence of central obesity.1933'37'67 However, population comparisons should be interpreted
with caution because our population was also shorter
(13 cm) than Caucasians. 68 This degree of stunting
may also be associated with different patterns in body
composition (i.e., elevated abdominal fat with higher
BMI) that are associated with increased risk of
CAD. 69
Sedentary lifestyles have been associated with an
increased risk of CAD. 7 0 In our study, fitness level
was significantly lower in the urban men and
women. Decreased fitness level was associated with
higher glucose levels in men. In addition, when we
adjusted for total body fat, decreased fitness levels
were associated with higher apo A-I concentrations.
This counterintuitive finding may be explained by
the highly significant association between decreased
fitness levels and increased body fat. Furthermore,
it has been reported that when diet and weight loss
are controlled for, no changes in apo A-I were
observed. 71
Finally, elevated glucose, triglyceride, and total
and VLDL cholesterol concentrations were higher
and HDL cholesterol and apo A-I levels were lower
in urban men compared with rural men. Rural-urban
differences in plasma parameters were not as striking
in women, for whom significant differences were
found for glucose and apo B levels. These ruralurban differences in plasma parameters were not
significant after adjustment for anthropometric measurements, smoking, age, and fitness level, suggesting
that elevated total and abdominal obesity, increased
cigarette smoking, and decreased fitness level explained in part the differences observed in plasma
parameters and blood pressure between urban and
rural men and women. These factors seem to contribute to the increased incidence of CAD observed
in several developing countries, particularly in the
urban areas. Our data are consistent with previous
reports on general and abdominal obesity and how
they relate to CAD risk factors. Additionally, we
report an increased prevalence of general and abdominal obesity, cigarette smoking, elevated systolic
and diastolic blood pressure, and decreased fitness
level in urban compared with rural Puriscal, particularly in men. The higher prevalence of such risk
factors in the urban area is associated with a more
atherogenic plasma lipoprotein profile.
Acknowledgments
We thank Leonardo Mata at the Instituto de
Investigaciones en Salud (INISA) for his support.
We also want to thank Marcela Vives, Edwin Quiros,
and the fieldworkers in the field station in Santiago,
Puriscal, for their assistance.
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KEY WORDS • body fat distribution • physical activity •
blood pressure • glucose • plasma lipoproteins • triglycerides
• cholesterol • apolipoproteins • low density lipoprotein
particle size
Downloaded from http://atvb.ahajournals.org/ by guest on June 15, 2017
Downloaded from http://atvb.ahajournals.org/ by guest on June 15, 2017
Relations of body habitus, fitness level, and cardiovascular risk factors including
lipoproteins and apolipoproteins in a rural and urban Costa Rican population.
H Campos, S M Bailey, L S Gussak, X Siles, J M Ordovas and E J Schaefer
Arterioscler Thromb Vasc Biol. 1991;11:1077-1088
doi: 10.1161/01.ATV.11.4.1077
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