Epicardial Fat from Echocardiography: A New ... - Wiley Online Library

Epicardial Fat from Echocardiography: A New Method for Visceral Adipose Tissue Prediction Gianluca Iacobellis,* Filippo Assael,† Maria Cristina Ribaudo,* Alessandra Zappaterreno,* Giuseppe Alessi,† Umberto Di Mario,* and Frida Leonetti*

Abstract IACOBELLIS, GIANLUCA, FILIPPO ASSAEL, MARIA CRISTINA RIBAUDO, ALESSANDRA ZAPPATERRENO, GIUSEPPE ALESSI, UMBERTO DI MARIO, AND FRIDA LEONETTI. Epicardial fat from echocardiography: a new method for visceral adipose tissue prediction. Obes Res. 2003;11:304 –310. Objective: To validate transthoracic echocardiography as an easy and reliable imaging method for visceral adipose tissue (VAT) prediction. VAT is recognized as an important indicator of high cardiovascular and metabolic risk. Several methods are applied to estimate VAT, with different results. Research Methods and Procedures: We selected 60 healthy subjects (29 women, 31 men, 49.5 ⫾ 16.2 years) with a wide range of body mass indexes. Each subject underwent transthoracic echocardiogram and magnetic resonance imaging (MRI) to measure epicardial fat thickness on the right ventricle. Measurements of epicardial adipose tissue thickness were obtained from the same echocardiographic and MRI views and points. MRI was also used to measure VAT cross-sectional areas at the level of L4 to L5. Anthropometric indexes were also measured. Results: Subjects with predominant visceral fat accumulation showed higher epicardial adipose tissue thickness than subjects with predominant peripheral fat distribution: 9.97 ⫾ 2.88 vs. 4.34 ⫾ 1.98 (p ⫽ 0.005) and 7.19 ⫾ 2.74 vs. 3.43 ⫾ 1.64 (p ⫽ 0.004) in men and women, respectively. Simple linear regression analysis showed an excellent correlation between epicardial adipose tissue and waist circumference (r ⫽ 0.895, p ⫽ 0.01) and MRI abdominal VAT (r ⫽ 0.864, p ⫽ 0.01). Multiple regression analysis showed that epicardial adipose tissue thickness (r2 ⫽ 0.442,

Received for review May 14, 2002. Accepted for publication in final form December 3, 2002. *Endocrinology, Department of Clinical Sciences, “La Sapienza” University, Rome Italy and †Radiology Department, Ospedale G. Vannini, Istituto Figlie di S. Camillo, Rome, Italy. Address correspondence to Gianluca Iacobellis, M.D., Clinica Medica 2, Dipartimento di Scienze Cliniche, Policlinico Umberto I, Viale del Policlinico 155, 00161 Roma, Italy. E-mail: [email protected] Copyright © 2003 NAASO

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p ⫽ 0.02) was the strongest independent variable correlated to MRI VAT. Bland test confirmed the good agreement between the two methods. Discussion: Epicardial adipose tissue showed a strong correlation with anthropometric and imaging measurements of VAT. Hence, transthoracic echocardiography could be an easy and reliable imaging method for VAT prediction.

Introduction Visceral obesity is recognized as an important risk factor for the development of all features of metabolic syndrome, such as insulin resistance, diabetes, dyslipidemia, and hypertension (1–9). Detection of visceral adipose tissue (VAT),1 which is the fat deposited around the internal organs, is a crucial issue for identifying visceral obesity. Nevertheless, it is difficult to obtain an accurate measurement and characterization of VAT. Several “simple” and “non-simple” methods are applied as surrogates for estimation of body composition and VAT. Anthropometric measurements are the most used, but are frequently imprecise (10). However, waist circumference is widely accepted as a good predictor of intra-abdominal fat mass (11). Sagittal diameter assessed by magnetic resonance imaging (MRI) shows advantages over waist circumference, but its ability to predict VAT is limited in obese subjects (12). Imaging techniques are certainly more precise and reliable than anthropometric measurements. Computed tomography (CT) and especially MRI, the gold standard technique, provide methods to estimate VAT safely and accurately (13–19). Unfortunately, both MRI and CT are quite high-cost methods, and CT requires radiation exposure. Recently, abdominal ultrasound measurement seems to provide a good and reproducible calculation of VAT, enhancing the ultrasonography as a promising technique for its low cost and easy

1 Nonstandard abbreviations: VAT, visceral adipose tissue; MRI, magnetic resonance imaging; CT, computed tomography; BMI, body mass index; FM, fat mass; SAT, subcutaneous adipose tissue; TAT, total adipose tissue; SAD, sagittal abdominal diameter; CI, confidence interval.

Epicardial Fat from Echocardiography, Iacobellis et al.

application (20 –23). Echocardiography, an ultrasound method frequently used in clinical management of patients with metabolic syndrome, may be applied to indicate VAT by epicardial adipose tissue detection. Hence, the aim of this study was the validation of transthoracic echocardiography as an accurate, easy, and reliable imaging method for VAT prediction.

Research Methods and Procedures Subjects We selected 60 healthy consecutive subjects (white, 29 females, 31 males, 49.5 ⫾ 16.2 years) with a body mass index (BMI) between 21 and 52 kg/m2 (median ⫽ 33), without hypertension, diabetes, dyslipidemia, and other metabolic diseases. A different group of 20 consecutive subjects (white, 10 females, 10 males, 50.4 ⫾ 14.5 years) with a BMI between 22 and 45 kg/m2 was used as a validation group. Both echocardiographic and MRI measurements were performed in these subjects during routine examinations. All subjects gave informed consent before the study began. Anthropometric Measurements Weight (to the nearest 0.1 kg) and height (to the nearest 0.5 cm) were measured while the subjects were fasting and wearing only their undergarments. BMI was calculated as body weight divided by height squared and was used as a marker of obesity degree. Minimum waist circumference (in centimeters) (minimum circumference between the lower rib margin and the iliac crest, midwaist) and maximum hip circumference (in centimeters) (the widest diameter over the greater trochanters) were measured while the subjects were standing with their heels together. We used waist circumference value (⬎88 cm in women and ⬎102 cm in men) as the threshold of predominant truncal/abdominal fat distribution (24). Subjects were subdivided, according to waist circumference value, into subjects with predominant visceral fat accumulation and with predominant peripheral fat accumulation. Impedensitometry Measurements Fat mass (FM) and free FM were estimated using a bioeletrical impedance analyzer following the manufacturer’s equations, which included data from obese and lean subjects (25). Echocardiographic Study Each subject underwent transthoracic two-dimensional guided M-mode echocardiogram. Echocardiograms were performed with a Siemens SONOLINE Omnia instrument (Issaquah, WA) by standard techniques with subjects in the left lateral decubitus position. Echocardiograms were recorded on videotape. The echocardiographic study required

recording of ⱖ10 cycles of two-dimensional parasternal long-and short-axis views and ⱖ10 cycles of M-mode with optimal cursor beam orientation in each view (26,27). Echocardiograms were preliminarily read by a first reader and subsequently reread by a highly experienced reader. Both readers were blinded to subjects’ anthropometric features. The coefficient of variation between the two different sonographers was 3%, indicating good reproducibility of the echocardiographic measurements. We excluded two subjects from 82 initially selected (2.5%) because of a technically unsatisfactory view. We measured epicardial fat thickness on the free wall of the right ventricle from both parasternal long- and short-axis views. Epicardial adipose tissue appears as an echo-free space (Figure 1). Measurement of epicardial fat on right ventricle was chosen for two reasons: 1) this point is recognized as the highest absolute epicardial fat layer thickness (28), and 2) parasternal long- and short-axis views allow the most accurate measurement of epicardial adipose tissue on the right ventricle with optimal cursor beam orientation in each view. Hypertrophy of the right ventricle trabecula and moderator band, even if it occurred, did not confound epicardial adipose tissue calculation (28). MRI Measurements The MRI studies were performed with a 1,5-T system (Gyroscan ACS-NT 1000, Philips, Eindhoven, The Netherlands) by using a body coil for signal transmission and reception. Respiratory triggering was used for the sequences, whereby repetition time was dependent on respiratory frequency. During the examination, patients were not given special breathing commands. The areas of abdominal VAT, subcutaneous adipose tissue (SAT), and total adipose tissue (TAT) were measured at the L4 to L5 level. We obtained turbo field echo T1weighted sequences with axial and sagittal orientation, antero-posterior phase encoding direction, 10-mm-thickness section with 1-mm intersection gap, 364 field of view, and a 256 ⫻ 256 matrix. The entire VAT and SAT volumes were measured by MRI while the subjects were lying supine on their abdomen, with arms elevated above the head, as described by Ross et al. (16). The SAT ⫹ VAT volumes were summed to obtain TAT volume. Then VAT was calculated as TAT-SAT. Epicardial adipose tissue scans (Figure 2) were obtained by turbo spin echo T1-weighted sequences with oblique axial orientation for a correct study of the four cardiac chambers, 10-mm-thickness section with 1-mm intersection gap, 370 field of view, and a 256 ⫻ 256 matrix. We measured epicardial fat thickness on the free wall of right ventricle, using the same echocardiographic points and views. The sagittal abdominal diameter (SAD) was measured at the L4 to L5 level. The intraclass OBESITY RESEARCH Vol. 11 No. 2 February 2003

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Figure 1: Transthoracic echocardiogram showing a large area of epicardial adipose tissue (white arrows) on free wall of right ventricle (RV).

correlation for repeated VAT, SAD, and epicardial adipose tissue determinations in our laboratory was 0.98. Statistical Analysis Data in the text and in the tables are expressed as mean ⫾ SD. Simple and multiple linear regression analyses were performed on all magnetic resonance, echocardiographic, anthropometric, and clinical variables to identify correlates of epicardial fat and MRI VAT. Mann-Whitney test with 95% confidence interval (CI) was applied to evaluate the differences between men and women. The Kruskall-Wallis test with 95% CI was used to evaluate the differences among the groups of patients with different conditions of fat tissue distribution in men and women, respectively. To assess the agreement between magnetic resonance and echocardiographic measurements we used the method described by Bland (http://www.mbland.sghms.ac.uk/ diffunit.htm). We started by regressing the measurement by the old method on the measurement by the new. This regression equation can be used to estimate a predicted old method measurement for any observed value by the new method. Of course, this gives the mean old method value for subjects with this new method value; it does not take the variation between subjects into account. We took this into account by calculating a range of possible values for the old method value on this subject, called a 95% prediction interval. One could then say for any observed test value an interval within which the gold standard would be with probability 95%. This gives us something akin to the limits of agreement. The width of the prediction interval is not 306


constant, being smallest near the middle of the range and wider as we get further toward the extremes. This effect is quite marked for small samples, but not for large. These prediction intervals form curves about the regression line. Two-tailed p ⬍ 0.05 indicated statistical significance. Analysis was done using Stata 5.0 (Stata Corp., College Station, TX).

Results Subject Characteristics Anthropometric and clinical characteristic of subjects studied, men and women, are summarized in Table 1. No significant difference with the subjects of the control group occurred. Echocardiographic Study of Epicardial Adipose Tissue The thickness of the epicardial adipose tissue on the right ventricle varies between 1.9 and 15.7 mm. No significant difference in epicardial adipose tissue between men and women was found (7.30 ⫾ 3.42 vs. 6.84 ⫾ 2.76). Subjects with predominant visceral fat accumulation showed higher epicardial adipose tissue thickness than subjects with predominant peripheral fat distribution: 9.97 ⫾ 2.88 vs. 4.34 ⫾ 1.98 (95% CI 4.05 to 7.21, p ⬍ 0.005) and 7.19 ⫾ 2.74 vs. 3.43 ⫾ 1.64 (95% CI 2.14 to 5.38, p ⬍ 0.004) in men and women, respectively. (Table 2). No significant differences in age and BMI among subjects with predominant visceral fat accumulation and subjects with peripheral fat occurred.


Figure 2: MRI showing epicardial adipose tissue, as T1-emphasized high signal density, on free wall of right ventricle and around left ventricular apex. TSET1-weighted sequence with oblique axial orientation, 10-mm thickness section with 1-mm intersection gap, 370 FOV, 256 ⫻ 256 matrix.

Correlates of Epicardial Adipose Tissue Simple linear regression analysis showed an excellent correlation between epicardial adipose tissue obtained from echocardiogram and MRI abdominal VAT measurement (Figure 3). Bland plot confirmed the good agreement between echocardiographic and MRI measurements (Figure 4). Epicardial adipose tissue was also related to waist circumference, epicardial fat from MRI, FM, SAD, and BMI, and hip circumference (Table 3). No correlation between epicardial adipose tissue measurement and age and sex was found. These correlations were substantially unchanged in the control group. Correlates of Waist Circumference Waist circumference showed a significant relationship with BMI (r ⫽ 0.744, p ⫽ 0.03) and SAD (r ⫽ 0.463, p ⫽ 0.05) in a univariate analysis taking into account the interaction among different covariates. No correlation between waist and either age or FM occurred. Correlates of MRI VAT Simple linear regression analysis showed that MRI VAT was significantly correlated with waist circumference (r ⫽ 0.798, p ⫽ 0.03), age (r ⫽ 0.421, p ⫽ 0.04), and FM (r ⫽

0.411, p ⫽ 0.05). No significant correlation between MRI VAT and BMI, MRI SAD, hip, and sex was found. Multiple regression analysis was performed to calculate the contribution of different covariates to the prediction of MRI VAT, taking into account sex as a dummy variable. Epicardial adipose tissue thickness and waist circumference were the strongest independent variables correlated to MRI VAT (Table 4). The relationship between epicardial adipose tissue and MRI VAT was unchanged taking into account the possible effect of BMI and age. Also in this case the data were substantially unchanged in the control group.

Discussion Our results showed that epicardial adipose tissue detected by echocardiography is strongly correlated with imaging and all anthropometric measurements of VAT. We have found an excellent correlation of epicardial adipose tissue with abdominal VAT estimated by MRI. Echocardiographic calculation of adipose tissue on the free wall of the right ventricle showed a good reliability with the MRI epicardial adipose tissue measurements. An excellent relationship between epicardial adipose tissue thickness and waist circumference also occurred in our subjects. Epicardial adipose tissue, a true visceral fat tissue, is deposited around the heart, particularly on the free wall of OBESITY RESEARCH Vol. 11 No. 2 February 2003

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Table 1. Body composition and visceral adipose tissue measures in men and women Men (n ⴝ 31) Age (years) 50.2 ⫾ 14.6 Height (m) 1.70 ⫾ 0.09 Weight (kg) 95.2 ⫾ 19.2 33.1 ⫾ 13.8 BMI (kg/m2) Waist (cm) 108.8 ⫾ 16.6 Hip (cm) 110.3 ⫾ 11.8 FAT (kg) 41.8 ⫾ 15.4 Free FM (kg) 52.7 ⫾ 16.4 Epicardial fat (cm) 7.30 ⫾ 3.42 MRI abdominal VAT (Liters) 2.01 ⫾ 0.9 MRI abdominal 213 ⫾ 99.4 VAT (cm2) MRI abdominal SAT (Liters) 3.7 ⫾ 1.8 MRI abdominal SAT (cm2) 392.4 ⫾ 130.1 MRI SAD (cm) 25 ⫾ 6

Women (n ⴝ 29)

p

47.7 ⫾ 15.4 1.58 ⫾ 0.09 82.5 ⫾ 18.8 33.7 ⫾ 14.9 104.5 ⫾ 15.4 116.9 ⫾ 13.2 37.8 ⫾ 21.6 45.1 ⫾ 17.2 6.84 ⫾ 2.76

NS ⬍0.05 ⬍0.05 NS NS NS NS NS NS

1.92 ⫾ 1.1

NS

203.3 ⫾ 104.5

NS

3.15 ⫾ 1.7

NS

333.8 ⫾ 144 23 ⫾ 6

NS NS

Data are presented as mean ⫾ SD. Statistical analysis was performed using the medians of values (Mann-Whitney test). NS, Not significant.

right ventricle and on the left ventricular apex, but also around the atria. An experimental study showed that epicardial adipose tissue should be considered an important cardiovascular and metabolic risk indicator (29). In fact, the authors reported that in young-adult guinea pigs, the rate of free fatty acid release by epicardial adipose tissue was

Figure 3: Scatter plot of echocardiographic epicardial adipose tissue vs. MRI VAT.

approximately twice that of the perirenal fat depots. Obesity was recognized to be the most common predisposing factor for the accumulation of excess epicardial fat (29). In fact, we observed that epicardial adipose tissue is related to BMI and FM. Nevertheless, our data suggest that body fat distribution, particularly abdominal fat tissue, is more strongly correlated to epicardial fat. This finding could have an embriogenetic reason. In fact, epicardial fat and intra-abdominal fat seem to be both originally in the brown adipose tissue of infancy. Epicardial fat around the right ventricle in our subjects was not correlated with the age, and previous autoptical studies on humans confirmed our data (28). The strong correlation of epicardial adipose tissue thickness with waist circumference enhanced the potential role of this echocardiographic parameter as an imaging predictor of VAT. In fact, waist circumference is widely accepted as a marker of indication of subjects with adverse metabolic profile and high cardiovascular risk. Moreover, waist circumference is positively correlated with abdominal fat content (30), and our data confirmed this finding. Nevertheless, sole waist circumference is not sufficient to distinguish VAT. In fact, we used MRI, the gold standard technique, as the validation method of VAT assessment by echocardiography. On MRI images, epicardial fat appears as T1-empha-

Table 2. Epicardial adipose tissue in different conditions of fat tissue distribution in men and women Men

Age (years) BMI (kg/m2) Epicardial fat (cm)

Women

Waist > 102 (n ⴝ 16)

Waist < 102 (n ⴝ 15)

Waist > 88 (n ⴝ 15)

Waist < 88 (n ⴝ 14)

50.7 ⫾ 13.5 33.7 ⫾ 9.2 9.97 ⫾ 2.88*

48.7 ⫾ 11.6 33.2 ⫾ 9.7 4.34 ⫾ 1.98

48.6 ⫾ 15.3 34.5 ⫾ 10.5 7.19 ⫾ 2.74†

46.7 ⫾ 19.1 32.7 ⫾ 9.71 3.43 ⫾ 1.64

Data are presented as mean ⫾ SD. Statistical analysis was performed using the medians of values (Kruskal-Wallis test). * p ⬍ 0.05. † p ⬍ 0.04.

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Table 4. Correlates of MRI VAT in all subjects: multiple regression analysis

Echo epicardial Waist Age FM BMI MRI SAD Hip Figure 4: The middle line is the regression line, and the upper and lower lines are the prediction limits. The SE of prediction is best estimated by 108% and 95% limits of agreement, which are ⫾1.96 ⫻ 108 ⫽ ⫾212. The regression is MRI ⫽ 6.38 ⫹ 54.9 ⫻ echo, and the MRI predicted from the echo will fall between 6.38 ⫹ 54.9 ⫻ echo ⫺ 212 and 6.38 ⫹ 54.9 ⫻ echo ⫹ 212. We can simplify these limits to: 6.38 ⫹ 54.9 ⫻ echo ⫺ 212 ⫽ 54.9 ⫻ echo ⫺ 206 and 6.38 ⫹ 54.9 ⫻ echo ⫹ 212 ⫽ 54.9 ⫻ echo ⫹ 218. For example, if the echocardiogram gives 10.0 mm, we predict that the MRI would give between 54.9 ⫻ 10.0 ⫺ 206 ⫽ 549 ⫺ 206 ⫽ 343 cm2 and 54.9 ⫻ echo ⫹ 218 ⫽ 549 ⫹ 218 ⫽ 767 cm2.

sized high-signal density. We found a strong correlation between epicardial adipose tissue and MRI VAT, suggesting that transthoracic echocardiography could be a very good technique to estimate VAT. Echocardiographic assessment of VAT could be an easy and effective method in the context of other ultrasound measurements. In fact, recently, several studies showed the effectiveness of ultrasonography as a precise and reliable method for evaluation of VAT, including prehepatic fat thickness (31). Some reports have described a good correlation between ultrasound measure-

Table 3. Correlates of echocardiographic epicardial adipose tissue in all subjects: simple regression analysis

MRI epicardial Waist MRI VAT FM MRI SAD BMI Hip Sex Age

R

p

0.905 0.895 0.864 0.655 0.645 0.597 0.479 0.355 0.212

0.00 0.01 0.01 0.01 0.01 0.05 0.03 0.09 0.11

t

p

2.95 2.24 1.77 1.54 1.01 0.42 0.32

0.02 0.02 0.06 0.09 0.11 0.18 0.23

R2 ⴝ 0.442

ments of intra-abdominal adipose tissue and CT images of VAT (22,24) and waist circumference (25), whereas others have not (23). Epicardial adipose tissue calculation by echocardiography requires very little time and can be easily applied during an examination for evaluation of morphological and functional cardiac parameters in patients with obesity, diabetes, and hypertension. However, a certain experience is necessary to measure epicardial adipose tissue thickness. In fact, epicardial adipose tissue may produce an echo-free space that can be mistaken for pericardial fluid (32–33). Hence, transthoracic echocardiography could be an accurate, easy, and reliable imaging method for VAT prediction. The possible association of epicardial adipose tissue measurement with metabolic and biochemical parameters needs further investigation.

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