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Subcutaneous fat: A better marker than visceral fat for insulin resistance in
obese adolescents

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DOI: 10.1016/j.clnme.2013.10.003

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 e-SPEN Journal 8 (2013) e251ee255

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journal homepage: http://www.elsevier.com/locate/clnu

Original article

Subcutaneous fat: A better marker than visceral fat for insulin

resistance in obese adolescents
Matteo Baldisserotto a, Durval Damiani c, Louise Cominato c, Ruth Franco c,
Arthur Lazaretti a, *, Pablo Camargo b, Fabiano Marques b, Rita Mattiello a, Giovanni Cerri c,
João Carlos Santana a
a
School of Medicine and Post-graduate Program in Pediatrics/Child Health, Pontifícia Universidade Católica do Rio Grande do Sul, Brazil
b
School of Medicine, Pontifícia Universidade Católica do Rio Grande do Sul, Brazil
c
School of Medicine, Universidade de São Paulo, Brazil

a r t i c l e i n f o s u m m a r y

Article history: Background & aims: Few studies have evaluated how well ultrasonographic measurements of fat
Received 28 June 2013 correlate with anthropomorphic measurements and insulin resistance in juveniles. Moreover, the sig-
Accepted 16 October 2013 nificance of an accumulation of visceral versus subcutaneous fat in obese children and young adults
remains controversial. The hypothesis of this study was that ultrasonographic measurements of fat
Keywords: would show better correlations with insulin resistance than with anthropometric measurements. Among
Subcutaneous fat
the variables associated with insulin resistance, we tried to identify those that had the best correlations
Abdominal
with ultrasonographic measurements of fat.
Intra-abdominal fat
Obesity
Methods: Forty-five adolescent volunteers (age range: 10e17 years) were enrolled in this study. Subjects
Ultrasonography were classified as obese or eutrophic according to their body mass index z-score for Brazilian children
Adolescent and adolescents. Blood samples and anthropometric measurements (waist circumference, waist-to-
Insulin resistance height ratio, and conicity index) were obtained from all subjects. All patients underwent an ultrasonic
assessment of subcutaneous tissue, pre-peritoneal fat, and intra-abdominal fat.
Results: Ultrasonographic measures of abdominal fat were associated with anthropometric measure-
ments, glucose level, insulin level, and the Homeostasis Model Assessment of Insulin Resistance (HOMA-
IR), with the exception that glucose level was not associated with the maximal pre-peritoneal fat. Body
mass index z-score, conicity index, and HOMA-IR remained independently associated with the subjects’
total fat in multivariate analysis. Only minimal subcutaneous fat was independently associated with
HOMA-IR.
Conclusion: Subcutaneous fat may be more useful than visceral fat as a marker for insulin resistance in
juveniles.
Ó 2013 European Society for Clinical Nutrition and Metabolism. Published by Elsevier Ltd. All rights
reserved.

1. Introduction global adiposity, body mass index (BMI) is widely recommended

for pediatric use.4 However, growing evidence indicates that the
Obesity is a major public health problem due to its growing risks for metabolic and cardiovascular diseases are determined by
prevalence1 and associated comorbidities,2 especially coronary both total fat and the fat distribution in the body.5,6 Additionally,
heart disease.3 As a simple and reasonably reliable indicator of

Abbreviations: BMI, body mass index; WC, waist circumference; WC:H, ratio between WC and height; CIx, conicity index; CT, computed tomography; MR, magnetic
resonance; US, ultrasonography; IAF, intra-abdominal fat; IR, insulin resistance; TG, triglycerides; TC, total cholesterol; HDL, HDL-cholesterol; LDL, LDL-cholesterol; ApoB,
apolipoprotein B; HOMA-IR, homeostasis model assessment of insulin resistance; Smax, maximum subcutaneous fat thickness; Smin, minimum subcutaneous fat thickness;
Pmax, maximum pre-peritoneal fat; Pmin, minimum pre-peritoneal fat; ICC, intraclass correlation coefficient; CI, confidence interval; SD, standard deviation.
* Corresponding author. Riveira Street, 520 Apartment 702, Porto Alegre 90670160, Brazil. Tel.: þ55 51 3279 3340; fax: þ55 54 3312 4747.
E-mail addresses: matteob@terra.com.br (M. Baldisserotto), durvald@iconet.com.br (D. Damiani), louise.cominato@hotmail.com (L. Cominato), ruthrocha@usp.br
(R. Franco), arthurlazaretti@yahoo.com.br, nefroped_lazaretti@yahoo.com.br (A. Lazaretti), pablo.camargo@gmail.com (P. Camargo), fabiano.s.marques@gmail.com
(F. Marques), rita.mattiello@pucrs.br (R. Mattiello), giovanni.cerri@hcnet.usp.br (G. Cerri), jocaped@pucrs.br (J.C. Santana).

2212-8263/$36.00 Ó 2013 European Society for Clinical Nutrition and Metabolism. Published by Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.clnme.2013.10.003
e252 M. Baldisserotto et al. / e-SPEN Journal 8 (2013) e251ee255
BMI may be a less reliable index of obesity in children than in
adults.
Waist circumference (WC) is a highly sensitive and specific
marker of upper body fat accumulation in children.7,8 Used alone or
in combination with stature, WC may offer a more sensitive means
than BMI for identifying overweight and obese children at
increased risk for developing metabolic complications.7 The WC-to-
height ratio (WC:H) is increasingly used to assess the risk of dis-
eases related to central fatness.7 The conicity index (CIx), related to
WC, height, and weight, appears to have a prognostic value in ju-
veniles that is similar to that of the waist-to-hip ratio in adults.9
Imaging methods, such as computed tomography (CT) and
magnetic resonance (MR), can reveal body fat distribution with
good accuracy. However, these techniques have disadvantages,
such as high cost, radiation exposure, and limited access by re-
searchers. Ultrasonography (US) has been proposed as an alterna-
tive, non-invasive technique for obtaining accurate measures of
subcutaneous and visceral fat thickness.10 Evaluations of intra-
abdominal fat (IAF) using US have been shown to correlate
strongly with visceral fat area measurements obtained by CT.11,12
Abdominal echography is a reliable and reproducible method to
quantify intra-abdominal adipose tissue and to diagnose intra-
abdominal obesity.13 Advantages of US methods include speed,
broad availability, and relatively low cost.14
Visceral fat thickness, as measured by US examination, has been
consistently correlated with total visceral fat and cardiovascular
risk factors.10 In multiple regression models, the addition of US
measurements improved estimates of visceral and subcutaneous
fat in adults compared to the contribution of standard anthropo-
metric variables.15 Furthermore, US measurements may associate
better with cardiovascular risk factors than do values derived from
anthropometric measures.16,17
Few studies have evaluated how well US measurements of fat
correlate with anthropomorphic measurements and insulin resis-
tance (IR) in juveniles. Moreover, the relative importance of an
accumulation of visceral versus subcutaneous fat in obese children
remains controversial.14 The hypothesis of this study was that US
measurements of fat would show better correlations with IR than
with anthropometric measurements. Among the variables associ-
ated with IR, we sought to identify those that had the best corre-
lations with US measurements of fat.
2. Materials and methods
2.1. Subjects
Two groups of subjects, 10e17 years of age, were enrolled in this
study: an obese group meeting the criterion for obesity according
to the BMI z-score for Brazilian children and adolescents,18 and a
eutrophic group consisting of subjects with BMIs not meeting that
obesity criterion. Exclusion criteria were hepatorenal disease, use of
drugs that are potentially hepatotoxic or nephrotoxic, and chronic
disease, such as hypertension or diabetes mellitus. Subjects were
evaluated in a pediatric outpatient clinic at either the Instituto da
Criança da Universidade de São Paulo in São Paulo or the Hospital
São Lucas da Pontifícia Universidade Católica do Rio Grande do Sul
in Porto Alegre. This research project was approved by the Research
Ethics Committee of both institutions. Parents or legal guardians
read and signed an informed consent form approved for this study
by the University’s Review Board.
2.2. Measurements
Individuals were weighed and measured according to stan-
dardized procedures19 while barefoot and wearing only light
clothing. For body weight determination, we used a mechanical
FilizolaÒ brand scale with a coupled stadiometer that was cali-
brated by the National Institute of Metrology, Standardization and
Industrial Quality of Rio Grande do Sul (INMETRO-RS). The BMI for
each subject was calculated as follows: BMI ¼ body weight (kg)/
height2 (m). For each subject, the WC was measured twice with an
anthropometric fiberglass tape at the midpoint between the last rib
and the iliac crest. The average of two measurements was recorded.
The WC:H ratio was determined by dividing WC (cm) by height
(cm). The CIx was calculated from the weight, height, and WC, using
the following equation:
Waist Circumference ðmÞ
C Index ¼ qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
0:109 Body weight ðkgÞ
Height ðmÞ
Blood pressure was measured with an aneroid sphygmoma-
nometer in accordance with the criteria recommended by the Na-
tional High Blood Pressure Education Program Working Group on
Children and Adolescents.20 Blood samples were obtained from all
subjects after 12 h of fasting. Glycemia, triglyceride (TG), total
cholesterol (TC), HDL-cholesterol (HDL), LDL-cholesterol (LDL), in-
sulin, and apolipoprotein B (apoB) levels were determined. TC, HDL,
and TG levels were measured enzymatically. LDL levels were
calculated using the Friedewald formula. The TC, LDL, HDL, and TG
values were stratified by percentile according to age and sex. In-
sulin and apoB levels were determined with chemiluminescence
and automated immunonephelometry, respectively. We calculated
the patients’ Homeostasis Model Assessment of Insulin Resistance
(HOMA-IR) index, a mathematical model that quantifies IR, based
on the formula: HOMA-IR ¼ fasting insulin (mUI/mL)  fasting
glucose (mmol/L)/22.5.
All patients received an US assessment of subcutaneous
tissue, pre-peritoneal fat, and intra-abdominal fat. Each patient’s
total fat was calculated according to the formula
Smax þ Smin þ Pmax þ Pmin þ IAF, where Smax, Smin, Pmax, and
Pmin are the maximum and minimum subcutaneous fat thickness
and pre-peritoneal fat, respectively. Measurements of these fat
layers are described below.
2.2.1. US of subcutaneous tissue, pre-peritoneal fat, and intra-
abdominal fat
We performed US examinations using an HD11 Philips machine
(Philips Medical Systems, Bothell, WA). The transducer was placed
on the skin gently to avoid compressing the fat beds. US mea-
surements of the subcutaneous, pre-peritoneal, and visceral
abdominal fat were performed with patients lying in a supine po-
sition. A 7.5e10-MHz linear transducer was maintained perpen-
dicular to the skin in the upper middle abdominal region as we
performed each exam longitudinally from the xiphoid process to
the umbilical region across the length of the linea alba, taking care
that the surface of the liver was nearly parallel to the skin.
Smax was measured 5 cm from the umbilicus on the umbilical
line. Smin was measured immediately below the xiphoid process.
We performed measurements directly from the screen, using an
electronic caliper on the skin-fat interface (excluding the skin) and
on the muscleefat interface, and then measured the average
thickness. Measurements of the maximum and minimum beds of
pre-peritoneal fat (Pmax and Pmin, respectively) were performed
in the region where the fat was most easily visualized, immediately
below the xiphoid process, between the internal side of the linea
alba and the surface of the liver. Finally, we used a 3.5e5.0-MHz
curvilinear transducer to measure the thickness of the visceral fat
bed, commonly referred to as IAF, between the internal side of the
abdominal muscle and the anterior wall of the aorta.
 M. Baldisserotto et al. / e-SPEN Journal 8 (2013) e251ee255 e253

To assess intra-observer agreement, one experienced radiologist Table 1

(MB) performed two measurements, separated by an interval of Characteristics of the patients (N ¼ 45).

one week, in a group of patients. When performing the second Characteristic Valuea
measurement, the observer was blinded to the results of the first Sex (no. females), no. (%) 24 (53)
measurement. The intraclass correlation coefficient (ICC) for the Nutritional status (no. obese), no. (%) 25 (56)
total fat was 0.961, with a 95% confidence interval (CI) of 0.851e Age (y) 13.06  2.34
0.990. BMI (kg/m2) 27.23  8.46
Median z-score BMI (25the75th 2.69 (0.15 to 3.26)
interquartile range)
2.3. Statistical analysis WC (cm) 90  20
WC:H 0.56  0.13
CIx 1.26  0.11
Demographic data are reported as means  standard deviation Pmax (cm) 1.03  0.36
(SD), for parametric variables, or medians with interquartile ranges, Smin (cm) 1.5  0.92
for non-normally distributed variables. We evaluated the intra- Pmin (cm) 0.46  0.27
Smax (cm) 1.88  1.12
observer agreement for the echograms through the ICC. General-
IAF (cm) 2.55  1.21
ized Linear Models were used to analyze the relationships between Total fat (cm) 7.35  3.39
the main outcomes (total fat) and the predictor variables (sex, age, ApoB (g/L) 0.63  0.15
height, weight, z-score BMI, WC, WC:H, CIx, and HOMA-IR index). TC, no. (%) patients below 75th percentileb 29 (64.4%)
In another multivariate analysis model, US fat measurements and HDL, no. (%) patients above 50th percentile 20 (46.5%)
LDL, no. (%) patients below 75th percentileb 31 (68.8%)
anthropometric measurements were taken as predictor variables TG, No. (%) patients above 75th percentile 14 (32.5%)
and HOMA-IR was taken as the outcome variable. Initially, all Insulin (pmol/L) 13.3  9.98
covariates that presented with p < 0.15 and with clinical relevance Glucose (mmol/L) 4.73  0.4
were included in the multivariate model. Covariates for which HOMA-IR 2.96  2.57
critical (i.e. not significant) p values were obtained were then Abbreviations: BMI, body mass index; WC, waist circumference; WC:H, ratio be-
excluded individually. This exclusion step was repeated until all tween WC and height; CIx, conicity index; Pmax, maximum pre-peritoneal fat;
variables remaining in the model presented had p values < 0.05. All Smin, minimum subcutaneous fat thickness; Pmin, minimum pre-peritoneal fat;
Smax, maximum subcutaneous fat thickness; IAF, intra-abdominal fat; ApoB,
analyses were performed with SPSS v.18 software (SPSS Inc, Chi- apolipoprotein B; TC, total cholesterol; HDL, HDL-cholesterol; LDL, LDL-cholesterol;
cago, IL). TG, triglycerides; HOMA-IR, homeostasis model assessment of insulin resistance.
a
Unless otherwise indicated, values are means  SDs.
b
Considered acceptable for age.
3. Results

The characteristics of the enrolled subjects are summarized in 4. Discussion

Table 1. The cohort was majority female (53%) and majority obese
(56%), with a mean BMI of 27.23  8.46 kg/m2 and a mean age of
13.06  2.34 years. The average anthropometric values and US
measurements of abdominal fat are reported in Table 1. About
two-thirds of the subjects in the study cohort had TC (64.4%) and
LDL (68.8%) levels below the 75th percentile (considered
acceptable for their age). However, nearly half (46.5%) of the
subjects had HDL levels above the 50th percentile for their sex
and age, and nearly a third (32.5%) had TG levels above the 75th
percentile.
Univariate analysis (Tables 2 and 3) indicated that our US
measurements of abdominal fat (Pmax, Smax, Pmin, Smin, IAF, and
the sum of these variables) were directly associated with the
following anthropometric measurements: BMI z-score, WC, WC:H,
and CIx. Additionally, blood glucose level, blood insulin level, and
HOMA-IR were associated directly with measures of abdominal fat,
with the exception that blood glucose was not associated with
Pmax. None of the fat measures had associations with gender or
height. Age was associated with all of the US fat measures, except
Pmax and Pmin.
In a multivariable model using the total fat as the outcome
variable and sex, age, BMI z-score, CIx and HOMA-IR as predictor
variables, the total fat was associated positively with the afore-
mentioned predictor variables, except for sex and age (Table 4). In
another multivariate analysis model, in which US fat measurements
were taken as predictor variables and HOMA-IR as the outcome
variable, only minimal subcutaneous fat was associated indepen-
dently with HOMA-IR (b ¼ 2.166; 95% CI, 1.633e2.699; p < 0.001).
In the linear regression model, minimum subcutaneous fat was
the variable with the highest r2 with the HOMA-IR index (0.614).
This US measurement of fat was superior to anthropometric mea-
surements (BMI z-score, waist/height ratio, CIx) and other fat
measurements, including IAF.
In the present study, we observed a direct association between
anthropometric and US measurements of fat in adolescents. Con-
troversy surrounds the practice of screening for adiposity in
childhood, given limited research showing that body composition
in childhood is directly related to adult health outcomes.9 Some
studies have associated anthropometric measurements (BMI, WC,
WC:H, and CIx) with US measures of abdominal fat in pediatric
patients and adolescents. However, the superiority of any of these
methods of quantifying fat over the others for this age band re-
mains controversial.
Stolk et al. found that abdominal US examination was a reliable
and reproducible method for quantifying IAF and diagnosing intra-
abdominal obesity in a group of moderately overweight Dutch
adults.13 Koot et al. showed that US was not more reliable than
anthropometry for assessing visceral fat in a group of severely
obese children and adolescents.21 Liem et al. showed that US did
not perform better than anthropometry in a group of 31 healthy
children.22 Gradmark et al. reported that BMI, WC:H, and WC
correlated with US measurements of superficial subcutaneous ad-
ipose tissue in a population-based cohort of Swedish adults. They
concluded that simple anthropometric measures of abdominal
obesity provided reasonably valid estimates of abdominal adiposity
in this population.23 In a longitudinal study performed by Reinehr
et al. on obese children, WC had a stronger relationship with car-
diovascular risk factors in obese children compared to US mea-
surements of intra-abdominal adipose tissue.5 In our study, all
anthropometric measures were predictive of US measurements of
abdominal fat. However, only Smin was superior to anthropometric
measures in predicting IR.
The pathogenic role of visceral fat in children appears to be
similar to that in adults, whereas the role of subcutaneous fat in
obesity in children appears to be different from that in adults.14
e254 M. Baldisserotto et al. / e-SPEN Journal 8 (2013) e251ee255

Table 2
Univariate analysis between subcutaneous and preperitoneal fat measured by US, anthropometric data, and HOMA-IR index.

Variable Pmax b (95% CI) p Smax b (95% CI) p Pmin b (95% CI) p Smin b (95% CI) p

Obese nutritional status 0.247 (0.050e0.445) .01 2.044 (1.775e2.313) <.001 0.361 (0.242e0.481) <.001 1.632 (1.385e1.879) <.001
BMI z-score 0.068 (0.020e0.115) .005 0.505 (0.442e0.568) <.001 0.096 (0.068e0.123) <.001 0.400 (0.340e0.460) <.001
WC 0.702 (0.212e1.192) .005 5.174 (4.541e5.808) <.001 1.018 (0.750e1.286) <.001 4.028 (3.401e4.654) <.001
WC:H 1.089 (0.325e1.852) .005 8.180 (7.286e9.075) <.001 1.541 (1.110e1.972) <.001 6.428 (5.545e7.310) <.001
CIx 0.952 (0.078e1.827) .03 7.192 (5.282e9.102) <.001 1.235 (0.644e1.827) <.001 5.576 (3.940e7.212) <.001
HOMA-IR 0.045 (0.002e0.089) .04 0.347 (0.258e0.435) <.001 0.068 (0.042e0.094) <.001 0.289 (0.218e0.360) <.001

Abbreviations: US, ultrasonography; BMI, Body Mass Index; WC, waist circumference; WC:H, the ratio between WC and height; CIx, conicity index; HOMA-IR, homeostasis
model assessment of insulin resistance; Pmax, maximum pre-peritoneal fat; Smax, maximum subcutaneous fat thickness; Pmin, minimum pre-peritoneal fat; Smin, minimum
subcutaneous fat thickness; IAF, intra-abdominal fat.

Table 3 In our study, only Smin was associated independently with

Univariate analysis between intra-abdominal fat and the total fat measured by US, HOMA-IR, corroborating the hypothesis that, in adolescents, sub-
anthropometric data, and HOMA-IR index. cutaneous fat may associate more closely with IR than visceral fat.
Variable IAF b (95% CI) p Total fat b (95% CI) p Tamura et al. studied 35 children, finding that Smin was weakly but
Obese 1.865 (1.414e2.317) <.001 6.082 (5.224e6.939) <.001
positively correlated with fasting serum insulin levels. Those au-
nutritional thors suggested a synergistic effect of subcutaneous fat on the
status development of hyperinsulinemia.14
BMI z-score 0.466 (0.358e0.574) <.001 1.520 (1.326e1.714) <.001 Our study has certain limitations. The sample size and cross-
WC 4.753 (3.689e5.818) <.001 15.535 (13.751e17.319) <.001
sectional design of the study limit the power of some analyses,
WC:H 7.677 (6.131e9.223) <.001 24.682 (22.300e27.064) <.001
CIx 7.089 (4.879e9.298) <.001 22.318 (16.927e27.709) <.001 such as the possible associations among laboratory data and the US
HOMA-IR 0.288 (0.162e0.413) <.001 1.021 (0.746e1.297) <.001 measures of fat. Furthermore, no functional measure of IR was
BMI, body mass index; WC, waist circumference; WC:H, the ratio between WC and
available in the study. IR can be quantified directly by two general
height; CIx, conicity index; HOMA-IR, homeostasis model assessment of insulin methods: the glucose clamp technique, and the measurement of
resistance; IAF, intra-abdominal fat. insulin-mediated changes in glucose disappearance rates after
intravenous glucose challenge (minimal model approach). These
methods provide precise quantitative measures of IR but are costly,
Although visceral fat is generally considered to be more strongly challenging to perform, moderately invasive, and best suited for
associated with metabolic risk factors than subcutaneous fat, studies involving tens to hundreds of individuals; thus, they are
nevertheless, subcutaneous fat may contribute to a greater absolute impractical for routine clinical use. During the time that we
risk due to its greater volume.4 collected our data, we were unable to determine the adolescents’
Some studies have found an equally strong or stronger asso- pubertal stage. Finally, we only had US measures of fat, and did not
ciation between subcutaneous abdominal adiposity and IR. measure fat by other techniques, such as CT or MRI. However, such
Lovejoy et al. reported that subcutaneous abdominal fat was other measurements were not the purpose of the study and have
significantly correlated with insulin sensitivity index and fasting several disadvantages.
insulin only among AfricaneAmerican women.24 In another On the basis of the findings from this study, it can be concluded
group of AfricaneAmerican women, subcutaneous adipose tissue that BMI and anthropometric measurements are associated with
had a greater effect on IR.25 In the Insulin Resistance Athero- US fat measurements, as well as with certain metabolic changes
sclerosis Study, subcutaneous fat, but not visceral fat, was posi- known to be associated with obesity-related morbidity. Our finding
tively associated with acute insulin response.26 Visceral fat was that subcutaneous fat measures were associated robustly with
not significantly correlated with any measure of insulin in a HOMA-IR values in obese adolescents suggests that subcutaneous
study of 20 black and 20 white normal-weight girls aged 7e10 fat may be a more useful marker than visceral fat for the devel-
years. However, serum insulin levels at baseline and after a 2-h opment of IR in this group. More studies in larger cohorts are
oral glucose tolerance test were significantly correlated with needed to confirm these results.
subcutaneous fat, as assessed by MRI in black girls.27 Abate et al.
concluded that subcutaneous truncal fat plays a major role in Sources of funding
obesity-related IR in men, whereas intra- and retro-peritoneal fat
have a lesser role.28 Goodpaster et al. showed that subcutaneous There has been no significant financial support for this work
abdominal fat and visceral fat had equally strong associations that could have influenced its outcome.
with IR in lean to obese subjects.29 Findings by Tershakovec et al.
suggest that subcutaneous fat quantity may be associated with IR Author contributions
in children.30
MB, GC, DD conceived and designed the study.
Table 4
MB, DD, LC, RF, PC, FM and JS collected the data.
Multivariable analysis between the total fat, anthropometric data, and HOMA-IR MB, AL and RM analyzed and did the interpretation of data; they
index. developed the article and revised it critically.
Variables Total fat b (95% CI) p
All authors read and approved the final manuscript.

BMI (z-score) 0.979 (0.719e1.240) <.001

CIx 6.736 (2.518e10.954) .002 Conflict of interest statement
HOMA-IR 0.296 (0.103e0.489) .003

BMI, body mass index; CIx, conicity index; HOMA-IR, homeostasis model assess- There are no known conflicts of interest associated with this
ment of insulin resistance. publication.
 M. Baldisserotto et al. / e-SPEN Journal 8 (2013) e251ee255 e255

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