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International Journal of Obesity (2005) 29, S97–S100

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PAPER
Adipose tissue and metabolic effects: new insight into
measurements
A Pietrobelli1*, AL Boner1 and L Tatò1
1
Pediatric Unit, Verona University Medical School, Verona, Italy

BACKGROUND: Epidemiologic evidence supports the theory that the relation between obesity and disease risk begins early in
life, and those risk factors for disease track, or remain at a similar level, with advancing age, growth, and development. The fat
tissue, once considered as a depot for energy substrate, is a metabolically active tissue. The fat cells produce agents that regulate
a host of physiological processes directly related to carbohydrate and fat metabolism and the development of cardiovascular
disease and type 2 diabetes.
AIM: To discuss fat tissue, and fat distribution in relation to body composition measurements, with particular emphasis on
imaging techniques (ie, dual energy X-ray absorptiometry (DXA), computed tomography (CT), and magnetic resonance
imaging (MRI)) and its relationship with metabolic and cardiovascular heath variables mediated by the metabolic characteristics
of the adipose tissue.
DISCUSSION: In sum, the medical and physiological health complications of childhood obesity are well documented. Imaging
methods are considered the most accurate means available for in vivo quantification at the tissue–organ level and the methods of
choice for calibration of field methods designed to measure adipose tissue.
International Journal of Obesity (2005) 29, S97–S100. doi:10.1038/sj.ijo.0803079

Keywords: body composition measurements; pediatric; body fat; visceral adipose tissue; subcutaneous adipose tissue

Introduction weight during the same period is about 260%. The


Obesity results when intake exceeds expenditure and both accumulation of FM is very rapid during the first 4–6 months
sides of the energy-balance equation must be considered in of life. As a percentage of fat-free mass (FFM), water decreases
concert in research on the etiology of childhood obesity.1 throughout infancy whereas protein and mineral increase.
Epidemiologic evidence supports the theory that the relation However, the quantitative nature of these changes remains
between obesity and disease risk begins early in life, and that uncertain. Recently, Fomon and Nelson4 revisited the body
risk factors for disease track, or remain at a similar level, with composition of the reference infant to permit initial
advancing age, growth, and development.2 estimates of the gain in energy and specific nutrients during
During growth, the human body increases in size and selected age intervals.
changes proportion of various components due to hormone The aim of our article is to discuss fat tissue, and fat
mediators.3 Growth is a complex, biological process regu- distribution in relation with body composition measure-
lated by multiple factors. These factors include genetic, ments, with particular emphasis on imaging techniques and
nutrition intake, physical activity, age, gender, and endo- their relationship with metabolic and cardiovascular health
crine balance, all of which influence a child’s height and variables mediated by the metabolic characteristics of the
body composition during the growth years. Clinical assess- adipose tissue.
ment of growth and nutritional status is enhanced by
accurate measurement of body composition. For a healthy
infant born at term, the average increase in fat mass (FM) Fat mass
during infancy, is about 600%, whereas the increase in body The fat tissue, once considered as a depot for energy
substrate, is a metabolically active tissue.5 The fat cells
produce agents that regulate a host of physiological
*Correspondence: Dr A Pietrobelli, Pediatric Unit, Verona University
processes directly related to carbohydrate and fat metabo-
Medical School, Policlinic GB. Rossi, Via delle Menegone 10, Verona
37134, Italy. lism6 and the development of cardiovascular disease and
E-mail: angpie@tin.it type 2 diabetes.2
Pediatric adipose tissue measurements
A Pietrobelli et al
S98
FM is the most variable component of body composition, visceral adipose tissue measurements in children available in
and between-individual variability ranges from approxi- the literature in order to analyze the effect of age, gender,
mately 6–60% of total body weight.7 At birth average FM pubertal status, and ethnicity and we found differences in
is about 10–15%, increases to 30% at 6 months of age total and regional adiposity due to ethnicity, gender, and
and graduallys decrease during early childhood.8 Between pubertal status relationship.18 Hormones per se also play a
5 and 8 y of age a ‘preadolescent’ wave or ‘adiposity rebound’ fundamental role in determining body fat distribution; in
occurs9 and then, in girls percent total fat increases from fact, earlier onset of puberty implies that the development of
an average of 20 to 26% between 9 and 20 y, while in an adult body fat pattern will occur at an accelerated way
boys it decreases from 17 to 13% after 13 y of age as FFM that may lead to earlier onset of adulthood diseases.2 Dietary
increases.10 factors and physical activity influence adipose tissue dis-
Two critical periods for the development of overweight in tribution in adults.19,20 Very few studies looked at these
pediatric age are the prenatal period and adolescence. Also relationships in children and it was found that in obese
‘adiposity rebound’ could be considered as the third.11 Both children aerobic training program influence changes in
low and high body mass appear to arise during the prenatal subcutaneous adipose tissue.21
period.12 Infants with high birth weight appear to have an Finally, regional adiposity, lipid and insulin action are
increased risk of subsequent overweight. Effects of the closely related. Changes in lipid and lipoprotein concentra-
intrauterine environment on cell numbers, satiety centers tions may result from insulin resistance and the accompany-
in the brain, and endocrine function represent mechanisms ing hyperinsulinemia in children and adolescents.14,15
that account for the apparent prenatal influence on
excessive weight at birth.13 Early adiposity rebound appears
associated with an increased risk of overweight in adulthood Fat measurements
as well as adolescence and represents the third critical period Although adipose tissue cannot be directly measured in
when overweight occur and may increase the risks of the living humans, various, indirect measures are available for
sequelae of obesity in adulthood.13 use with children and adolescents.1 These measures include
Measures of body composition and total body fatness the body mass index (BMI: weight in kg/height in m2), and
change with growing, developing, and aging. Specific cutoff weight for-stature indexes, skinfold measures, electrical
values for children and adolescents have been suggested bioimpedance analysis, dual energy X-ray absorptiometry
based on specific health-related criteria. However, defining (DXA) and imaging techniques (magnetic resonance ima-
obesity standards in children and adolescents remains ging (MRI); and computed tomography (CT)).22 We review in
controversial, and widely accepted percent body fat (%BF) detail DXA and MRI, while emphasizing the importance of
criteria have not yet to be developed. Several studies reported assessment of fat distribution in children and adolescents.
the relationship between adiposity and metabolic risk factors
in children and adolescents.2,14,15
Dual energy X-ray absorptiometry
DXA quantifies the relative attenuation of two main photon
Fat distribution peaks as they pass through tissue. The relative attenuation of
Fat distribution refers to the relative amount of fat in the the two discrete photon streams is a function of tissue
primary compartments where adipose tissue and fat are elemental composition. This phenomenon can be described
stored in the body.16 The anatomical distribution of adipose using the ratio (R-value) of low to high photon energy
tissue shows distinct patterns of change with age and gender attenuation. The R-value at any given energy for each
maturation. Regional fat represents a single variable as element is known and constant.23,24 Bone, rich in calcium
subcutaneous adipose tissue or visceral adipose tissue. and phosphorous, has a high relative attenuation and R-
Subcutaneous adipose tissue is referred to as ‘fat patterning’ value; fat, which is mainly low atomic number hydrogen and
to distinguish it from visceral adipose tissue, the accumula- carbon, has a low relative attenuation and low R-value; and
tion of internal adipose tissue.16 In general, subcutaneous lean soft tissue with oxygen and electrolytes have an
adipose tissue increases in the trunk in boys during intermediate R-value.23 Systems conceptually measure each
adolescence and gluteal femoral tissue increases in girls. pixel’s R-value as they pass over regions of the whole body
These changes are associated with stage of sexual matura- and then reconstruct three compartments, bone mineral
tion, sex hormone levels, and changes in plasma lipid or content, FM, and FFM using manufacturer-specific recon-
lipoprotein cholesterol concentration.17 struction algorithms (Figure 1).23 The use of DXA to assess
Several other factors influence both visceral and subcuta- body composition in children and youth is an ideal one
neous adipose tissue. Total FM is an important determinant and it is a valid method to track changes over time. DXA
of visceral adipose tissue, but it is not completely clear estimates of bone mineral, soft tissue, and fat are not greatly
whether increasing adiposity in children and adolescents is affected by the hydration level of FFM. Theoretical analysis24
related to increasing visceral adipose tissue.2 Recently, we showed that the natural variation in FFM hydration alters
pooled together all the data on MRI subcutaneous and DXA estimates of percent fat less than 1%.

International Journal of Obesity


Pediatric adipose tissue measurements
A Pietrobelli et al
S99
and cardiovascular disease.30 Using imaging we could under-
stand the origin of the significant relationship between
Fat
visceral adipose tissue and adverse health and also explain
the influence of ethnic and gender differences in adipose
tissue distribution.18
MRI for pediatric body composition measurement is
Soft-Tissue relatively new and the lack of radiation exposure associated
Water with its use makes it more applicable than CT. On the other
Body
hand, MRI is to our knowledge the only method in vivo used
Weight Lean to study fetal body composition31 and it could help to
understand the physiological and pathological condition in
Proteins the newborn. The reproducibility of MRI for subcutaneous
adipose tissue in the infant is between 2.4 and 4.0% and
Glycogen approximately 17% for visceral adipose tissue.32 As we noted
Minerals before, tissue composition may vary with age, and in
Bone neonates fat content of adipose tissue is 66% and gradually
Minerals increases to 80% at the age of 13 y.33
The most common use of MRI in body composition
Figure 1 Dual energy X-ray absorptiometry model. Modified from refe- research is the measurement of abdominal adipose tissue
rence 23.
distribution, and this technique is capable of distinguishing
between subcutaneous and visceral adipose tissue. Thus, we
This technique has the potential to substantially improve could provide new insight into the relationship between
the feasibility of body composition analysis with children for abdominal obesity and related comorbidities.34
whom other laboratory techniques may be impractical (eg, A single slice or several slices could be obtained. One scan
underwater weighing). The greatest advantage of DXA may is sufficient to determine fat tissue area, whereas several scan
be the ability to assess regional body composition (trunk, slices are needed to estimate fat tissue volume. A single scan
arms, and legs). Nutritional status of diseased individuals can at the L4–L5 or umbilicus level is typically used to measure
be evaluated by analyzing the individual compartments of visceral and subcutaneous abdominal fat areas.29 Advances
the body. We propose that DXA has great potential as both a in the measurement of internal as well as subcutaneous
pediatric research tool and a clinical tool if the specific adipose tissue with MRI allow investigators to study
characteristics of the system being used are recognized.22 An compartments that were undistinguishable (ie, intrathoracic
example of a research use of DXA that may lead to clinical and intra-abdominopelvic areas) and could help to under-
application is the prediction of comorbidity risk in obese stand relations with metabolic factors.16
children and adolescents.25 In prepubertal children, a cutoff
point of 33% body fat estimated by DXA had a good
sensitivity to identify an adverse risk factor profile.25 Studies Comments and conclusion
showed that a greater than 30% body fat lipid profile In sum, the medical and physiological health complications
worsens in girls.26,27 In boys, a 20% body fat26 and a 25% of childhood obesity are well documented. Children who
body fat27 were suggested as cutoffs for obesity in children were at risk for overweight or who were overweight were 2.4
and adolescents based on cardiovascular disease risk. times as likely as normal weight children to have elevated
DXA measures total abdominal fat and may provide a total cholesterol, diastolic blood pressure, low-density lipo-
strong index, but this technique cannot resolve subcuta- protein cholesterol, high-density lipoprotein cholesterol,
neous from intra-abdominal adipose tissue,1 although Loh- systolic blood pressure, triglycerides, and fasting insulin.35
man28 suggested that DXA abdominal fat in combination Several of these associations differed between white and
with skinfold thicknesses could be used to estimate intra- black subjects, and by age.36 The association of central
abdominal fat. adiposity with the mentioned risk factors is clearly stronger
for obese children and adolescents. Imaging methods are
considered the most accurate means available for in vivo
Imaging quantification at the tissue–organ level and the methods of
Computerized axial tomography (CT) and MRI provide choice for calibration of field methods designed to measure
investigators with the opportunity to evaluate tissue-system adipose tissue.
level components in vivo.29 In particular, accumulation of It is fundamental to underline that an enlarged abdomen
visceral adipose tissue is related with adverse health and the and an higher amount of trunk fat deposition in obese
effect of fat distribution on disease risk is a fundamental children and adolescents are consistently related with a
issue.30 In children and adolescents, recent studies found a deterioration of lipid and metabolic profiles.16 In children
correlation between central fat and type 2 diabetes mellitus and adolescents, insulin sensitivity and hyperinsulinemia

International Journal of Obesity


Pediatric adipose tissue measurements
A Pietrobelli et al
S100
are independently related to circulating lipid after adjusting 18 Brambilla P, Bedogni G, Moreno LA, Goran MI, Gutin B, Fox KR,
for adiposity and this relation could be exacerbated by Peters DM, Barbeau P, De Simone M, Pietrobelli A. Cross-
validation of anthropometry against magnetic resonance ima-
high accumulation of intra-abdominal fat.2 Using imaging
ging for the assessment of visceral and subcutaneous adipose
techniques, a tremendous variation in the amount of tissue in children. Int J Obes Relat Metab Disord 2006, in press.
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accumulate in early childhood. This implies that to be Goran MI. Dietary fat in relation to body fat and intra-abdominal
adipose tissue: a cross sectional analysis. Am J Clin Nutr 1996; 64:
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dietary intake, and physical activity: effects on body fat
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19991; 53: 1104–1111.
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International Journal of Obesity


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