Open Journal of Endocrine and Metabolic Diseases, 2012, 2, 63-69 Published Online November 2012 (
Evaluation of Visceral and Subcutaneous Fat by
Ultrasound and Its Relationship with Clinical and
Metabolic Parameters of Insulin Resistance and
Subclinical Atherosclerosis
Clarisse Miranda Prado, Germana Augusto de Vasconcelos, Emmanuelle Tenorio A. M. Godoi,
Érica Nogueira Bezerra Cavalcanti, Tiago Matos de Arruda, Erik Trovão Diniz,
Cynthia Salgado Lucena, Luiz Griz, Francisco Bandeira
Hospital Agamenon Magalhães, SUS/Universidade de Pernambuco, Recife, Brasil
Received September 1, 2012; revised October 3, 2012; accepted November 5, 2012
Objective: this study set out to investigate the association between abdominal obesity ultrasound measurements, waist
circumference and body mass index (BMI), metabolic syndrome (MS) components and subclinical atherosclerosis.
Methods: sixty patients were recruited and divided equally into two groups, according to the presence of MS. All sub-
jects had an ultrasound examination for measurement of visceral and subcutaneous fat thickness and carotid IMT. Re-
sults: the values of visceral fat thickness, preperitoneal circumference and carotid IMT were higher in patients with MS
than in control subjects. Visceral fat thickness showed significant correlations with many cardiovascular risk factors
(waist circumference, BMI, fasting plasma glucose, HDL and LDL cholesterol). All abdominal obesity measurements
were correlated with BMI. Carotid IMT showed correlations with age, visceral fat and preperitoneal circumference.
Visceral fat was independently associated with systolic and diastolic blood pressures and fasting plasma glucose. Sys-
tolic and diastolic blood pressures and BMI were independent determinants of carotid IMT. Conclusion: visceral fat
thickness showed the best correlation with MS components, suggesting that it could be a useful parameter in cardio-
vascular risk assessment. Age, systolic and diastolic blood pressures and BMI were independent determinants of sub-
clinical atherosclerosis. MS was associated with a higher carotid IMT.
Keywords: Visceral Fat Thickness; Subcutaneous Fat Thickness; Preperitoneal Circumference; Carotid Intima-Media
Thickness; Metabolic Syndrome
1. Introduction
A strong association has been shown between the meta-
bolic syndrome (MS) and an increased risk of cardiovas-
cular and total mortality [1-4]. Individuals with MS have
a higher risk of stroke and coronary artery disease [5,6].
The carotid intima-media thickness (IMT) is an estab-
lished indicator of atherosclerosis and is used as a surro-
gate marker for cardiovascular morbidity and mortality
[7-10]. Recent studies have shown an association be-
tween MS and increased carotid IMT [11,12].
Although obesity is recognized as an important risk
factor for cardiovascular disease (CVD) [13], the greatest
challenge is to identify measurements of obesity that best
reflect an increased risk of developing MS [14]. Ab-
dominal fat, represented by subcutaneous and visceral
adipose tissue, has been associated with MS [15,16].
However, there is still controversy as to whether these
measurements provide additional information on the
complications of MS [17].
This study aimed to investigate the association be-
tween abdominal obesity ultrasound measurements, waist
circumference and body mass index (BMI), on the one
hand, and MS components and subclinical atherosclero-
sis, on the other.
Some components, such as multi-leveled equations,
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create these components, incorporating the applicable
criteria that follow.
2. Methods
This was a cross-sectional study, which involved 60
patients treated on an outpatient basis at Agamenon
Magalhães Hospital, Recife, from March to July 2008.
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The inclusion criterion was age between 20 and 80 years
and the exclusion criteria were use of antiretroviral drugs,
chronic use of glucocorticoids and pregnancy. The study
was approved by the hospital’s Ethics Committee, and all
patients gave their written consent. Patient identification
data, medication use, disease history and results of labo-
ratory tests performed less than a month prior to the
interview, as well as measurements of the patients’ blood
pressure, waist circumference, weight, height and BMI
were recorded. Blood pressure was measured in the right
and left arms using the mercury sphygmomanometer
with the patient seated after 5 minutes’ rest. Patients who
had smoked at least one cigarette per day during the
previous six months were considered smokers.
A. Laboratory tests: a venous blood sample was
collected after a fast of at least 12 hours to measure
fasting blood glucose and serum lipids. The results were
obtained by the dry-slide method, using the Vitros 950
Chemistry System (Ortho-Clinical Diagnostics, Johnson &
Johnson Company).
B. Ultrasound measurements: the equipment used was
a Philips En Visor C (Bothell, USA). The abdominal
ultrasound was performed by two specialists, but all
measurements of carotid IMT were performed by a
single operator and those of intra-abdominal fat by
another. Neither operator had any information on the
patients’ clinical and laboratory data.
The measurement of carotid IMT was performed with
the patient in the supine position, using a 5.0 to 10.0
MHz linear array transducer. Three IMT measurements
were made in the plaque-free section of both the right and
left common carotid arteries, along the thickest point on
the far wall and within ~1.5 cm proximal to the flow
divider. The sonographic vascular lumen-intima transi-
tion was selected as the internal measurement site and the
media-adventitia transition as the external one. An average
of six measurements was used for the other calculations
The measurement of visceral and subcutaneous fat was
performed with a 2.0 to 5.0 MHz linear array transducer
along the midline of the abdomen, between the xiphoid
process and the umbilicus. The subcutaneous fat was
measured between the skin-fat interface (excluding the
skin) and the outer surface of the abdominal rectus
muscle. The visceral fat was measured between the inner
face of the rectus muscle and the posterior wall of the
abdominal aorta [19]. The two measurements were
repeated three times, following which the mean of the
measurements was calculated for each type of fat. The
preperitoneal circumference was calculated using the for-
mula: PC = AC (2π × SCF)/PC = preperitoneal
circumference/AC = abdominal circumference/SCF =
subcutaneous fat [20].
Definition of SM: We used the revised definition of
the National Cholesterol Education Program (NCEP) and
Adult Treatment Panel III (ATP III) [21]. The diagnosis
of MS was made in the presence of at least three of the
following five criteria: 1) waist circumference: 102 cm
in men and 88 cm in women; 2) triglycerides 150
mg/dl or patients using fibrates or nicotinic acid; 3) HDL < 40
mg/dl in men and <50 mg/dl in women or patients using
fibrates or nicotinic acid; 4) systolic blood pressure 130
mmHg or diastolic blood pressure 85 mmHg or pa-
tients using an antihypertensive drug; and 5) fasting plas-
ma glucose 100 mg/dl or use of hypoglycemic me-
Statistical analysis: Continuous variables were expressed as
mean and standard deviation and categorical variables as
percentages. The Student t-test was used to compare
groups of continuous variables and the chisquare test for
proportions. Pearson’s correlation was used to examine
the associations between the ultrasound measurements
themselves and between these and the epidemiological
and metabolic parameters. Multiple regression was used
to establish the independent contribution of the ultra-
sound to each component of MS. The same procedure
was also used to identify independent determinants of
carotid IMT, using the latter as a dependent variable. All
tests were performed using the program SPSS (Statistical
Package for the Social Sciences) for Windows, version 13.
P-values < 0.05 were considered statistically significant.
3. Results
The characteristics of the subjects are shown in Table 1.
Sixty patients, of whom 48 were females and 28 had a
diagnosis of diabetes mellitus (DM), were evaluated. The
60 participants were divided equally into two groups,
according to the presence or absence of MS. The group
of MS patients, when compared with the group without
MS, had a higher mean age, higher values for waist circum-
ference, BMI, fasting plasma glucose and triglycerides,
and lower levels of HDL cholesterol. The use of anti-
hypertensive and hypoglycemic drugs and statins was
also higher among the patients with MS. Visceral fat, pre-
peritoneal circumference and carotid IMT were signi-
ficantly higher in the MS patients. The subcutaneous fat
showed no significant differences between groups.
Table 2 shows that, among the measurements of
abdominal fat, visceral fat showed a higher positive
correlation with cardiovascular risk factors, presenting an
association with BMI, waist circumference, fasting
plasma glucose, HDL and LDL cholesterol. The subcu-
taneous fat was correlated with BMI and waist circumfe-
rence. The preperitoneal circumference was related to
BMI, waist circumference and HDL cholesterol. Waist
circumference was correlated with fasting plasma glu-
cose and BMI. Thus, all measurements of central obesity
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Table 1. Clinical and laboratory characteristics of the population according to presence or absence of MS.
With metabolic syndrome Without metabolic syndrome
Mean ± standard deviation Mean ± standard deviation
Age (years) 54.1 ± 11.02 46.4 ± 14.03 p(1) = 0.026*
Female, N (%) 23 (76.7%)** 25 (83.3%)** p
(2) = 0.519
Smoking, N (%) (current/ex) 10 (33.3%) 5 (16.7%) p(2) = 0.136
Waist circumference (cm) 98.6 ± 11.73 88.7 ± 12.77 p(3) = 0.003*
BMI (Kg/m2) 28.9 ± 4.19 25.7 ± 5.08 p(3) = 0.009*
Systolic blood pressure (mmHg) 132.8 ± 20.79 123.5 ± 15.76 p(1) = 0.055
Diastolic blood pressure (mmHg) 81.2 ± 12.84 78.7 ± 10.17 p(1) = 0.407
Use of antihypertensive, N (%) 27 (90.0%) 11 (36.7%) p(2) < 0.001*
Fasting plasma glucose (mg/dl) 133.6 ± 66.08 99.2 ± 42.18 p(1) = 0.022*
Use of hypoglycemic, N (%) 19 (63.3%) 6 (20.0%) p(2) = 0.001*
Total cholesterol (mg/dl) 183.7 ± 47.16 196.8 ± 42.70 P(3) = 0.264
HDL cholesterol (mg/dl) 39.3 ± 10.65 56.9 ± 14.56 p(3) < 0.001*
Triglycerides (mg/dl) 264.6 ± 371.70 103.7 ± 47.46 p(1) = 0.025*
LDL cholesterol (mg/dl) 106.0 ± 35.81 119.1 ± 39.24 p(3) = 0.189
VLDL cholesterol (mg/dl) 43.0 ± 62.87 20.8 ± 9.45 p(3) = 0.061
Use of statin, N (%) 13 (43.3%) 5 (16.7%) p(2) = 0.024*
Visceral fat (cm) 5.38 ± 1.89 4.44 ± 1.47 p(1) = 0.035*
Subcutaneous fat (cm) 2.16 ± 0.97 2.20 ± 2.12 p(1) = 0.925
Preperitoneal circumference (cm) 85.03 8.15 74.91 12.41 p(1) < 0.001*
Carotid intima-media thickness (mm) 0.69 ± 0.14 0.58 ± 0.12 p(1) = 0.001*
*Significant difference at 5.0%; **The percentages were based on 30 patients in each group; (1)Using the student t-test with equal variances; (2)Using the pearson
chi-square test; (3)Using the student t-test with unequal variances.
Table 2. Pearson’s corr elation coefficients significantly different from zero betw een ultrasound me asures and sever al selected
variables (metabolic syndrome group).
Waist circumference
circumference Visceral fat Subcutaneous fat Carotid IMT
Age Ns Ns ns ns 0.499 (<0.001)
BMI* 0.830 (<0.001) 0.573 (<0.001) 0.474 (<0.001) 0.414 (0.001*) ns
Waist circumference --------- 0.661 (<0.001) 0.615 (<0.001) 0.533 (<0.001) ns
FPG* (mg/dl) 0.263 (0.044) Ns 0.325 (0.012) ns ns
HDL Ns 0.449 (<0.001) 0.262 (0.043) ns ns
LDL Ns Ns 0.296 (0.024) ns ns
Visceral fat --------- 0.591 (<0.001) --------- ns 0.339 (0.008)
Subcutaneous fat ---------- 0.284 (0.028) --------- --------- Ns
Carotid IMT ---------- 0.285 (0.027) --------- --------- ---------
Values are expressed as R (p). *Body mass index; **Fasting plasma glucose.
were correlated with BMI. Total cholesterol, triglycerides,
VLDL cholesterol and systolic and diastolic blood
pressure showed no correlation with either waist circum-
ference or any ultrasound measurements, including ca-
rotid IMT. When the correlation of the parameters with
one another measured by ultrasound was analyzed, pre-
peritoneal circumference showed no correlation with any
other measurements, while carotid IMT was correlated with
visceral fat and preperitoneal circumference.
Multiple linear regression was performed to assess
which of the measurements of central obesity and BMI
were most closely related to the criteria for MS (Table 3).
Visceral fat was independently associated with blood
pressure and fasting glucose, while subcutaneous fat
showed an independent association with HDL cholesterol.
Preperitoneal circumference, BMI and waist circum-
ference were not correlated with any of the dependent
variables analyzed.
In assessing the independent contribution of compo-
nents of MS, BMI and measurements of abdominal fat to
carotid IMT, linear regression revealed that the levels of
systolic and diastolic blood pressure and BMI were de-
terminants of carotid IMT, regardless of the values of
triglycerides, HDL, fasting blood sugar, and ultrasound
measurements of abdominal obesity (Table 4).
4. Discussion
In this study, patients with MS had a higher mean age,
waist circumference, BMI, fasting plasma glucose and
triglycerides, and lower levels of HDL cholesterol than
those without MS. Several studies corroborate these
findings [7,8,22,23]. The blood pressure levels were not
higher in the MS group, which can be explained by the
greater use of antihypertensive drugs. In a cohort study
conducted in Finland [24], there was likewise no
statistical difference between the blood pressure levels of
patients with and without MS but, unlike our study, there
was no statistical significance between patients regarding
the use of antihypertensive drugs.
The correlation between MS and greater values for
carotid IMT has been repeatedly demonstrated [22-25],
and the number of components of the syndrome has been
related to an increase in carotid IMT [8].
All ultrasound measurements were significantly higher
in the presence of the syndrome, except for subcutaneous
fat, showing that intra-abdominal fat is the principal
parameter related to the MS. Its value may be obtained
directly, by measurement of visceral fat, or indirectly, by
measurement of the preperitoneal circumference. The
lack of association between subcutaneous fat and MS
was observed in a study conducted with 290 subjects in
China, in which the subcutaneous fat values were not
significantly higher in patients with MS, and multivariate
logistic regression did not demonstrate any independent
association of fat with the syndrome [16].
When the relationship between the measurements of
abdominal fat was evaluated, it was observed that ab-
dominal obesity ultrasound measurements were correlated
with the anthropometric measurements, waist circum-
ference and BMI. These findings are in agreement with
data from the literature [26,27]. Visceral fat was the one
that presented a significant correlation with the greatest
number of components of MS, with the exception of
blood pressure and triglycerides levels. This, however,
changed with linear regression, in which visceral fat was
correlated with the blood pressure levels, maintaining the
relationship with fasting plasma glucose, regardless of
sex, age, BMI and the other measurements of abdominal
fat. Furthermore, abdominal circumference, BMI, and
preperitoneal circumference were not correlated with any
component of the syndrome. These findings suggest that
visceral fat is the measurement of central obesity that is
best correlated with the risk factors analyzed. This
superiority of visceral fat over subcutaneous fat was also
Table 3. Coefficients of multiple linear regression of the individual components of MS, using anthropometric data as inde-
pendent variables, adjusted for gender and age (metabolic syndrome group).
Independent variables
Dependent variables BMI Waist circumference Subcutaneous fatPreperitoneal
circumference Visceral fat R-value2
SBP(1) ** ** ** **
2.39 (0.124) 0.155
DBP ** ** ** **
2.28 (0.018*) 0.113
TG(1) ** ** ** ** **
HDL ** **
0.46 (0.006*) ** **
FPG ** ** ** **
10.58 (0.012*) 0.106
*Significant at 5.0%; **Variable excluded by the method of backward selection with p < 0.15. (1)Remained the only constant in the model. Note: Values in
brackets represent the probability of significance of each variable.
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Table 4. Coefficients of linear regression of carotid IMT in
terms of ultrasound and anthr opometry measurements and
components of the SM, adjusted for sex and age (metabolic
syndrome group).
Independent variables Dependent variable: carotid IMT
SBP 0.002 (0.062)
SPD 0.006 (0.001*)
TG **
HDL **
Fasting plasma glucose
Waist circumference **
BMI 0.008 (0.015*)
Preperitoneal circumference **
Visceral fat **
Subcutaneous fat **
R-value2 R2 = 0.458
*Significant at 5.0%; **Variable excluded by the method of backward selec-
tion with p < 0.15. Note: Values in brackets represent the probability of
significance of each variable.
superiority of visceral fat over subcutaneous fat was also
evaluated in a study conducted in Turkey, which found
that visceral fat may play an important role in the
physiopathology of MS [28]. A study with 177 volun-
teers in Spain showed that preperitoneal circumference
was strongly correlated with all components of MS [29],
whereas in our study there was no correlation with any of
them. Moreover, the preperitoneal circumference was
considered better than visceral fat. This difference be-
tween the results can be explained by the fact that, in the
Spanish study, visceral fat was measured differently and
was considered synonymous with preperitoneal fat.
On linear regression analysis, performed to assess the
determinants of subclinical atherosclerosis, blood pres-
sure and BMI showed a positive correlation with carotid
IMT, regardless of sex, age, abdominal obesity ultra-
sound measurements, anthropometric parameters and
components of MS. Therefore, in this study, general
obesity was more correlated than central obesity with
subclinical atherosclerosis. In the study by Fadini and
colleagues, waist circumference and blood pressure were
independently correlated with carotid IMT [30], while in
the study by Kawamoto, age, male gender, systolic blood
pressure, HDL, LDL, smoking, diabetes mellitus and MS
showed an independent association with carotid IMT [9].
Scuteri, in a prospective study, found that age, male
gender, LDL and fasting plasma glucose were inde-
pendent factors associated with this measurement [7]. It
may therefore be stated that the relationship between the
components of MS and carotid IMT is still controversial,
but factors such as age [16], blood pressure levels [31]
and BMI [20] may be important determinants in several
studies, including our own.
This study had a number of limitations. It did not
determine a temporal relationship between obesity, MS
and subclinical atherosclerosis. Furthermore, the popula-
tion studied was relatively small and composed largely of
women. Prospective studies with a larger number of
participants of both genders are therefore required to
confirm our data.
In conclusion, visceral fat was the measurement of
abdominal fat that showed the best correlation with
markers of MS, suggesting that it can be used as a useful
parameter in assessing cardiovascular risk. Age, blood
pressure and BMI were independently associated with
subclinical atherosclerosis. The presence of MS was re-
lated to a higher carotid IMT, emphasizing that early
detection and control of MS should be part of strategy to
be employed in the prevention of CVD.
5. Acknowledgements
No competing financial interest exists. The authors have
no potential conflicts of interest to be disclosed.
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