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Risk Factors and Chronic Disease

Evaluation of Risk Profiles by Subcutaneous Adipose Tissue Topography in Obese Juveniles Reinhard Moeller,* Renate Horejsi,* Stefan Pilz,† Nicole Lang,† Karine Sargsyan,† Roumiana Dimitrova,† Erwin Tafeit,* Albrecht Giuliani,‡ Gunter Almer,† and Harald Mangge†

Abstract MOELLER, REINHARD, RENATE HOREJSI, STEFAN PILZ, NICOLE LANG, KARINE SARGSYAN, ROUMIANA DIMITROVA, ERWIN TAFEIT, ALBRECHT GIULIANI, GUNTER ALMER, AND HARALD MANGGE. Evaluation of risk profiles by subcutaneous adipose tissue topography in obese juveniles. Obesity. 2007;15:1319 –1324. Objective: To compare subcutaneous adipose tissue topography (SAT-top) in obese juveniles with age-matched normal-weight controls. Research Methods and Procedures: The optical device LIPOMETER (European Patent EP 0516251) enables the non-invasive, rapid, safe, and precise measurement of the thickness of subcutaneous adipose tissue. Fifteen defined body sites (1 ⫽ neck to 15 ⫽ calf) characterize the individual SAT-top like an individual fingerprint. SAT-top of 1351 juveniles (obese: 42 boys, 59 girls, normal weight: 680 boys, 570 girls) from 7 to 19 years of age were measured. For visual comparison, the 15-dimensional SAT-top information was condensed by factor analysis into a two-dimensional factor plot. Results: Both female and male obese juveniles had markedly increased adipose tissue layers at 7 ⫽ upper abdomen, 8 ⫽ lower abdomen, 5 ⫽ front chest, and 6 ⫽ lateral chest. The pubertal changes of body shape and fat distribution of the normal-weight boys and girls (boys show thinner adipose tissue layers on their legs, whereas girls had thicker adipose tissue layers at the extremities) were not seen in the

Received for review July 20, 2006. Accepted in final form November 13, 2006. The costs of publication of this article were defrayed, in part, by the payment of page charges. This article must, therefore, be hereby marked “advertisement” in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. *Institute of Physiological Chemistry, Center for Physiological Medicine, †Clinical Institute of Medical and Chemical Laboratory Diagnosis and Pediatric Rheumatology/Immunology, and ‡Department of Obstetrics and Gynecology, Medical University Graz, Graz, Austria. Address correspondence to Renate Horejsi, Institute of Physiological Chemistry, Center for Physiological Medicine, Medical University Graz, Harrachgasse 21/II, A-8010 Graz, Austria. E-mail: [email protected] Copyright © 2007 NAASO

obese group. Independently of age and sex, all of the obese juveniles showed a similar, more android body fat distribution with increased trunk fat. Discussion: SAT-top of the obese juveniles is similar to that of patients with type 2 diabetes, polycystic ovary syndrome, and coronary heart disease. Patients with these metabolic disorders and obese juveniles are located in the factor plot in the same area. This body shape may indicate a risk profile for developing polycystic ovary syndrome (women), type 2 diabetes, and early atherosclerosis (both sexes). Key words: metabolic diseases, body fat distribution, childhood obesity, adolescence

Introduction The prevalence of childhood obesity has been increased 4-fold during the last 20 years (1–3). Juvenile obesity, defined as a BMI ⬎95th percentile (4), is a strong risk factor for obesity in adulthood. Obese persons are at increased risks for fertility disorders, atherosclerosis (5), and psychological burdens (6). Subcutaneous abdominal adipose tissue is strongly related to insulin resistance in a manner similar to that of visceral adiposity (7). BMI values of juveniles correlate with increased fasting insulin levels, insulin resistance, dyslipidemia, and hypertension. However, because of growth, BMI is an inadequate measure in childhood and provides no information on body fat percentage or distribution (8). Data showing the subcutaneous adipose tissue topography (SAT-top)1 should render information about growth-dependent body fat distribution. Techniques such as magnetic resonance imaging, computed tomography, and DXA can accurately measure the thicknesses of subcutaneous adipose tissue layers, but allow radiation exposure, are expensive, and are difficult to handle (9,10). The LIPOMETER (European Patent EP 0516251) has been developed for non-invasive, fast, precise, and safe

1 Nonstandard abbreviations: SAT-top, subcutaneous adipose tissue topography; SAT, subcutaneous adipose tissue; PCOS, polycystic ovary syndrome.

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Evaluation of Risk Profiles, Moeller et al.

Table 1. Basic results for SAT-top measurements for male juveniles by age group (mean ⫾ SD) Age (years)

Controls 9.70 ⴞ 1.17

Obese 9.95 ⴞ 0.78


Obese 12.00 ⴞ 1.31


Obese 15.98 ⴞ 0.93

N 151 10 374 23 155 9 Height (cm) 139.59 ⫾ 8.63 148.65 ⫾ 6.62 156.06 ⫾ 11.37 161.53 ⫾ 9.82 176.34 ⫾ 6.85 178.06 ⫾ 7.88 Weight (kg) 34.18 ⫾ 6.75 60.81 ⫾ 13.78* 46.00 ⫾ 11.65 84.49 ⫾ 21.28* 66.10 ⫾ 8.77 105.76 ⫾ 11.52* 2 17.55 ⫾ 2.60 27.51 ⫾ 3.20* 18.93 ⫾ 2.13 32.62 ⫾ 3.18* 21.29 ⫾ 1.65 33.36 ⫾ 4.12* BMI (kg/m ) 1 ⫽ neck 4.1 ⫾ 2.6 12.6 ⫾ 4.0* 4.4 ⫾ 3.4 16.5 ⫾ 5.0* 3.2 ⫾ 1.6 14.9 ⫾ 3.5* 2 ⫽ triceps 7.9 ⫾ 2.4 16.2 ⫾ 3.2* 7.6 ⫾ 3.3 16.5 ⫾ 3.5 4.7 ⫾ 1.9 10.6 ⫾ 2.7 3 ⫽ biceps 4.3 ⫾ 2.3 12.7 ⫾ 5.4 4.1 ⫾ 2.6 12.0 ⫾ 3.5 2.7 ⫾ 1.1 10.4 ⫾ 4.7 4 ⫽ upper back 4.1 ⫾ 2.9 16.4 ⫾ 3.9* 4.0 ⫾ 3.1 16.9 ⫾ 4.6* 2.7 ⫾ 1.0 9.7 ⫾ 4.5* 5 ⫽ front chest 5.7 ⫾ 4.6 19.4 ⫾ 8.5 5.8 ⫾ 4.8 25.2 ⫾ 6.0* 3.7 ⫾ 2.0 20.0 ⫾ 6.1* 6 ⫽ lateral chest 3.8 ⫾ 3.3 17.4 ⫾ 3.2* 4.1 ⫾ 3.7 20.5 ⫾ 6.7* 3.0 ⫾ 1.9 18.5 ⫾ 6.1* 7 ⫽ upper abdomen 5.7 ⫾ 4.9 17.6 ⫾ 2.9* 5.7 ⫾ 5.1 15.2 ⫾ 3.4* 3.9 ⫾ 2.8 11.6 ⫾ 4.0* 8 ⫽ lower abdomen 7.0 ⫾ 5.0 18.2 ⫾ 4.6* 6.6 ⫾ 5.0 15.5 ⫾ 4.0 4.1 ⫾ 2.5 11.8 ⫾ 1.8 9 ⫽ lower back 6.9 ⫾ 4.0 15.8 ⫾ 4.3 6.7 ⫾ 4.1 14.4 ⫾ 3.5 5.2 ⫾ 2.0 11.5 ⫾ 3.9 10 ⫽ hip 6.4 ⫾ 4.8 19.5 ⫾ 5.2 6.2 ⫾ 4.9 17.7 ⫾ 3.6 4.5 ⫾ 2.9 15.6 ⫾ 4.4* 11 ⫽ front thigh 5,8 ⫾ 2,4 12,9 ⫾ 4,1* 5,4 ⫾ 2,7 9.9 ⫾ 3,7 3.2 ⫾ 1,5 6.8 ⫾ 2,8* 12 ⫽ lateral thigh 6.6 ⫾ 2.6 12.0 ⫾ 4.2 6.3 ⫾ 2.6 9.1 ⫾ 2.5 3.8 ⫾ 1.5 6.8 ⫾ 2.8 13 ⫽ rear thigh 5.1 ⫾ 2.1 8.6 ⫾ 3.0 4.6 ⫾ 2.1 7.3 ⫾ 2.7 3.0 ⫾ 1.2 4.7 ⫾ 1.5 14 ⫽ inner thigh 7.2 ⫾ 3.1 12.2 ⫾ 4,7 6.9 ⫾ 3.4 9.9 ⫾ 3.1* 4.1 ⫾ 2.2 7.4 ⫾ 2.4 15 ⫽ calf 4.5 ⫾ 1.7 7.9 ⫾ 2.0* 4.2 ⫾ 1.7 5.9 ⫾ 2.4* 2.6 ⫾ 0.9 4.1 ⫾ 1.3 * Significant differences (p ⬍ 0.01) compared with controls.

determination of subcutaneous adipose tissue (SAT) thickness. Fifteen specified measuring points provide an individual profile of SAT-top (11). LIPOMETER studies in patients with type 2 diabetes (12–14), polycystic ovary syndrome (PCOS) (15,16), or women with a history of weight cycling (17) showed that these persons have increased subcutaneous fatty tissue layers on their trunks, with comparatively thin layers on their extremities. Obese juveniles of all age groups show significant enlarged intima media thicknesses of the common carotid arteries. Adiponectin was significantly decreased, and resistin was increased (18). The aims of this study were to compare SAT-top profiles in obese juveniles and age-matched normal-weight controls, to describe an assumed altered sexual differentiation in the obese group, and to describe similarities in body fat distribution between obese juveniles and adults with type 2 diabetes, coronary heart disease, and/or PCOS. Thus, new risk profiles may be defined.

Research Methods and Procedures Subjects Study participants were part of the Styrian Juvenile Obesity Study, which was designed to investigate early athero1320


sclerosis and metabolic disorders in obese juveniles. The study was approved by the Ethics Committee of the Medical University of Graz, and all participants and their parents gave written informed consent. SAT-top was measured in 42 obese boys and 59 obese girls and 1250 normal-weight controls (680 boys and 570 girls) recruited from schools in urban areas. Weight and height were measured with a precision weighing balance (Tanita HD 372; Tanita Corp., Arlington Heights, IL) and a stadiometer. Obesity was defined as BMI ⬎95th percentile (4). The whole dataset was divided into three age groups: 9 years (7 to 11 years), 13 years (11 to 15 years), and 17 years (15 to 19 years). A description of SAT-top development through different age groups and the differences between girls and boys has been reported (19). The juveniles had no special diet and only the regular sport programs offered in schools (three lessons per week). SAT-top The thickness of subcutaneous tissue layers was measured with the LIPOMETER at 15 specified body sites for rendering a detailed SAT-top profile. The sensor head of the LIPOMETER contains a set of light-emitting diodes (␭ ⫽ 660 nm) and a photodetector. To measure the thickness of the SAT layer, the sensor head is held perpendicularly to the


Table 2. Basic results for SAT-top measurements for female juveniles by age group (mean ⫾ SD) Age (years)


Obese 9.21 ⴞ 1.04


Obese 13.09 ⴞ 0.3


Obese 16.70 ⴞ 1.29

N 140 13 301 25 129 21 Height (cm) 139.91 ⫾ 9.28 139.65 ⫾ 6.90 156.06 ⫾ 9.17 160.20 ⫾ 6.06 166.41 ⫾ 7.19 164.52 ⫾ 8.00 Weight (kg) 34.15 ⫾ 8.13 50.73 ⫾ 10.47* 46.82 ⫾ 10.83 78.85 ⫾ 12.35* 58.73 ⫾ 10.01 90.67 ⫾ 17.73* 2 17.42 ⫾ 2,58 25.2 ⫾ 3.46* 19.26 ⫾ 2.96 30.8 ⫾ 4.67* 21.2 ⫾ 2.33 33.45 ⫾ 4.17* BMI (kg/m ) 1 ⫽ neck 5.0 ⫾ 3.7 14.6 ⫾ 6.5 5.9 ⫾ 4.0 15.9 ⫾ 5.9 7.1 ⫾ 4.1 16.8 ⫾ 5.5 2 ⫽ triceps 9.3 ⫾ 3.3 15.1 ⫾ 3.1 9.4 ⫾ 3.1 16.0 ⫾ 4.7 11.7 ⫾ 4.6 19.9 ⫾ 3.4 3 ⫽ biceps 5.1 ⫾ 2.7 10.0 ⫾ 3.0 5.2 ⫾ 2.6 10.8 ⫾ 3.3 5.9 ⫾ 3.9 13.7 ⫾ 3.8 4 ⫽ upper back 5.2 ⫾ 4.3 16.3 ⫾ 5.6* 5.4 ⫾ 3.5 15.8 ⫾ 4.3* 6.2 ⫾ 3.6 16.7 ⫾ 3.4* 5 ⫽ front chest 5.6 ⫾ 5.3 19.3 ⫾ 7.1 7.3 ⫾ 4.8 19.6 ⫾ 6.5* 9.1 ⫾ 6.2 22.6 ⫾ 5.8 6 ⫽ lateral chest 5.3 ⫾ 4.7 16.2 ⫾ 5.5 5.5 ⫾ 4.1 18.0 ⫾ 5.1* 6.7 ⫾ 4.8 20.9 ⫾ 4.3* 7 ⫽ upper abdomen 7,6 ⫾ 5,9 19,0 ⫾ 4,6* 8,3 ⫾ 5,6 14,7 ⫾ 3,8* 10,7 ⫾ 5,9 15,0 ⫾ 5,3* 8 ⫽ lower abdomen 8.3 ⫾ 5.2 20.0 ⫾ 4.6 8.7 ⫾ 4.6 14.4 ⫾ 4.2 9.3 ⫾ 4.0 16.2 ⫾ 4.9 9 ⫽ lower back 8.8 ⫾ 5.0 16.1 ⫾ 3.5 8.9 ⫾ 4.1 13.7 ⫾ 3.7* 10.5 ⫾ 4.6 16.8 ⫾ 5.5 10 ⫽ hip 8.5 ⫾ 5.8 21.0 ⫾ 2.9 7.9 ⫾ 4.6 16.7 ⫾ 5.0 9.5 ⫾ 6.0 19.8 ⫾ 5.5 11 ⫽ front thigh 7.0 ⫾ 2.7 12.7 ⫾ 3.4* 7.2 ⫾ 2.4 10.7 ⫾ 3.5* 8.2 ⫾ 2.4 13.1 ⫾ 3.2* 12 ⫽ lateral thigh 7.9 ⫾ 2.5 11.7 ⫾ 4.1 7.9 ⫾ 2.3 9.5 ⫾ 3.1 8.7 ⫾ 2.4 11.7 ⫾ 2.9 13 ⫽ rear thigh 5.4 ⫾ 2.1 7.9 ⫾ 2.6 5.3 ⫾ 1.6 6.4 ⫾ 2.5 5.7 ⫾ 2.0 7.5 ⫾ 2.7 14 ⫽ inner thigh 7.9 ⫾ 2.8 12.9 ⫾ 4.1 8.8 ⫾ 3.1 10.8 ⫾ 3.9 9.7 ⫾ 3.7 13.6 ⫾ 3.8 15 ⫽ calf 4.2 ⫾ 1.6 5.0 ⫾ 1.3 4.5 ⫾ 1.4 4.6 ⫾ 1.7 4.9 ⫾ 1.6 5.9 ⫾ 2.6 * Significant differences (p ⬍ 0.01) compared with controls.

selected body site. The SAT layer is illuminated by different light patterns varying in time. A photodiode measures the corresponding back-scattered light intensities of these light patterns and calculates the thickness of the SAT layer in millimeters. Technical characteristics of the device and an initial validation of the results using computed tomography as a reference have been reported (20). The validity of the LIPOMETER and bioelectric impedance analysis for body fat in adults and children and additional comparison with skinfold calipers in children was studied by Jurimae et al. (21,22). To describe the complete subcutaneous body fat distribution, 15 evenly distributed and anatomically well-defined body sites were specified from 1 ⫽ neck to 15 ⫽ calf on the right side of the body. The complete measurement cycle takes ⬃2 minutes and is performed with the subject in an upright standing position. Statistics Data were analyzed with SPSS for Windows (SPSS, Inc., Chicago, IL). The hypothesis of variables being normally distributed was tested by the Kolmogorov-Smirnov test. Differences in the distribution of variables between obese and normal-weight children were tested with the Student’s t

test for independent samples in case of normally distributed variables (Table 1) and by the Mann-Whitney U test if variables were not normally distributed (Table 2). A value of p ⬍ 0.01 was considered to be statistically significant. Stepwise linear discriminant analysis was applied to study whether the knowledge of single SAT layers or the combination of SAT layers enables a correct classification between the different groups. Factor values were calculated to compare obese juveniles with other subjects (healthy juveniles as controls, adults, patients with metabolic disorders, etc.). Condensed SATtop information was visualized by a factor plot. The calculation of factor values has been reported (14).

Results SAT distribution differed markedly in both sexes for normal-weight juvenile controls in all age ranges. With increasing age, the adipose tissue layers decreased in male juvenile controls at all body sites. Fat loss was markedly pronounced in normal-weight boys between 9 and 17 years of age. Normal-weight girls developed a gynoid body fat distribution, characterized by thicker layers at the femoral region beginning at the age of 9 years. OBESITY Vol. 15 No. 5 May 2007

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Figure 1: SAT-top plot of obese (black bars) and normal-weight (gray area) boys and girls, showing the SAT deviation between these two groups. The body sites were sorted top-down from 1 ⫽ neck to 15 ⫽ calf.

In contrast, both female and male obese juveniles showed significantly thicker adipose tissue layers on their trunks at 5 ⫽ front chest, 6 ⫽ lateral chest, and 7 ⫽ upper abdomen. The body sites 5 ⫽ front chest and 6 ⫽ lateral chest were most pronounced in obese boys of all age groups, and gynecomasty was common. Obese girls (9 years) had significantly thicker SAT layers on the legs compared with obese boys and normal-weight juveniles in all age groups. The obese teenage girls (13 and 17 years) had similar thicknesses of adipose tissue layers on their legs as the age-matched control group. Table 1 contains the values of SAT-top of normal-weight and obese boys according to the age groups. The data of the girls are shown in Table 2. Figure 1 represents a graphical comparison of SAT-top and body fat profiles in normalweight vs. obese boys and girls.

Discussion Previous studies have shown that trunk obesity is frequently associated with metabolic disorders (18,23,24). Similar high-risk patterns of adipose tissue distribution were found in women with PCOS, men and women with type 2 diabetes and coronary heart disease, and female weight cyclers (13,15,17). Factor analysis especially combined with SAT-top plots yield new risk profiles of the individual SAT distribution. In 1322


the factor plot (Figure 2), patients with PCOS, type 2 diabetes, or coronary heart disease, and women with a history of weight cycling are in the same square (14,16). Obese juveniles may already have a comparable body fat distribution with trunk obesity as adults with advanced metabolic disorders. After calculating the factor values of all juveniles, the three age groups of boys (boys 9 years ⫽ m09, boys 13 years ⫽ m13, boys 17 years ⫽ m17, obese boys 9 years ⫽ mob09, obese boys 13 years ⫽ mob13, obese boys 17 years ⫽ mob17) and girls (girls 9 years ⫽ f09, girls 13 years ⫽ f13, girls 17 years ⫽ f17, obese girls 9 years ⫽ fob09, obese girls 13 years ⫽ fob13, obese girls 17 years ⫽ fob 17) were depicted in the extended factor value plot (Figure 2). The factor value plot represents an approach to visualize the 15-dimensional SAT-top space in a 2-dimensional diagram. Normal-weight children and juveniles are positioned on the left side of the factor plot (m09, m13, m17, f09, f13, and f17). Factor 1, related to the upper body SAT development, is below zero, which occurs in the age group of 9- and 13-year normal-weight girls (f09 and f13) and all normal-weight boys from 9 to 17 years (m09 to m17). All of them show thin trunk adipose tissue layers. During puberty, normal-weight boys lose fat on their legs, indicated by positions on the y-axis in the factor plot (Factor 2 ⬍ 0), whereas the normal-weight girls develop a gynoid pattern with thicker fat layers on the legs (Factor


Figure 2: The factor plot shows the correlation of female juveniles and adults from 9 to 80 years of age (f09 to f80), male juveniles and adults from 9 to 80 years of age (m09 to m80), male (T2DMm) and female (T2DMf) patients with type 2 diabetes and coronary heart disease (CHDm, CHDf), lean (PCOle) and obese (PCOob) women with PCOS, persons with extremely thin fatty tissue layers all over their body sites (anorexia and body builders), and male (mob09, mob13, mob17) and female (fob09, fob13, fob17) obese juveniles at the age groups of 7 to 11, 11 to 15, and 15 to 19 years.

2 ⬎ 0). In contrast, all obese juveniles showed increased fat layers on their trunk. Thus, Factor 1 is greater than zero in obese girls and boys who are on the right side of the factor plot. Because of thicker fat layers on their legs, obese juveniles are found in the middle and upper part of the right side of the factor plot, whereas adult patients with manifest metabolic disorders have thinner extremities, and, therefore, they are located in the factor plot at the right lower corner. Notably, the obese juveniles of all age groups do not show the typical pubertal change in SAT distribution seen in the normal-weight juveniles. They keep thick fat layers on their trunks, independently of age and/or pubertal stage. Trunk obesity, graphically shown as Factor 1, moves the obese juveniles to a position in the right field of the factor plot. The adipose tissue layers on their extremities are in a comparable range as the normal-weight controls and not yet as thin as in adult patients with metabolic diseases (obese patients with polycystic ovaries, coronary heart disease, type 2 diabetes). The dataset, gained by SAT-top using the LIPOMETER together with advanced statistical methods (factor plot), can be used to detect risk profiles, even in children and juveniles, which resemble the profiles of patients with clinically overt metabolic disorders.

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