Ultrasound in Med. & Biol., Vol. 40, No. 6, pp. 1083–1088, 2014 Copyright Ó 2014 World Federation for Ultrasound in Medicine & Biology Printed in the USA. All rights reserved 0301-5629/$ - see front matter

http://dx.doi.org/10.1016/j.ultrasmedbio.2013.12.017

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Original Contribution VISCERAL ADIPOSE TISSUE IS A BETTER PREDICTOR OF SUBCLINICAL CAROTID ATHEROSCLEROSIS COMPARED WITH WAIST CIRCUMFERENCE LOUKIANOS S. RALLIDIS,* KYRIAKI BAROUTSI,y MARIA ZOLINDAKI,z MARIA KARAGIANNI,y CHRISTOS VAROUNIS,* NIKOLAOS DAGRES,* JOHN LEKAKIS,* and MARIA ANASTASIOU-NANA* * Second Department of Cardiology, Attikon Hospital, School of Medicine, University of Athens, Athens, Greece; y Department of Radiology, General Hospital of Nikea, Piraeus, Greece; and z Biochemistry Department, General Hospital of Nikea, Piraeus, Greece (Received 10 September 2013; revised 8 December 2013; in final form 11 December 2013)

Abstract—We investigated whether visceral adipose tissue (VAT) measured by ultrasonography is better than waist circumference (WC) in predicting the presence of subclinical carotid atherosclerosis. We recruited 100 individuals without a history of cardiovascular disease or diabetes mellitus. VAT volume was measured by ultrasonography and common carotid artery intima-media thickness (CCA-IMT) by B-mode ultrasonography. Both VAT and WC were positively associated with body mass index, triglycerides, uric acid, systolic/diastolic blood pressure and high sensitivity C-reactive protein and inversely correlated with high-density lipoprotein cholesterol. However, only VAT was associated with CCA-IMT (r 5 0.309, p 5 0.002). Multivariate logistic regression analysis revealed that VAT, but not WC, was an independent predictor of carotid plaques after adjustment for cardiovascular risk factors (odds ratio [OR] 5 1.017, 95% confidence interval [CI] 5 1.003–1.031, p 5 0.017), and this association persisted after additional adjustment for WC (OR 5 1.024, 95% CI 5 1.003–1.031, p 5 0.027). Our data suggest that VAT volume measured by ultrasonography may be a better predictor of subclinical carotid atherosclerosis than waist circumference in healthy individuals. (E-mail: [email protected]) Ó 2014 World Federation for Ultrasound in Medicine & Biology. Key Words: Intima-media thickness, Visceral adipose tissue, Ultrasonography, Waist circumference.

Waist circumference (WC), a simple anthropometric marker, is currently the most commonly used measurement for AO (Klein et al. 2007). WC is considered a surrogate measure of VAT, and there are data suggesting that WC is associated with the risk of developing CVD (Balkau et al. 2007; Siren et al. 2012). However, WC is also largely influenced by the patient’s total adiposity and cannot be used to distinguish VAT from SAAT. It has been suggested that WC might have a weaker association with atherosclerosis than the VAT (Despres et al. 2008; Kim et al. 2009). Therefore, it is important to have a simple and tolerable method for the quantification of VAT. Currently, ultrasonography, a convenient and widely available method, is used for estimation of VAT (Shuster et al. 2012). However, it is not clear whether this measurement is better than WC in assessing cardiovascular risk. Seibert et al. (2013) suggested that ultrasound-measured VAT is probably unnecessary for assessing cardiovascular risk because this information can be obtained by the simpler measurement of WC.

INTRODUCTION Abdominal obesity (AO), a growing health problem worldwide, has been associated with glucose intolerance, hypertension, dyslipidemia, hyperinsulinemia and cardiovascular disease (CVD) (Despres et al. 2008; Fujioka et al. 1987; Lyon et al. 2003; Tchernof and Despres 2013). The association between AO and cardiometabolic risk factors is believed to be due mainly to excess visceral adipose tissue (VAT), whereas subcutaneous abdominal adipose tissue (SAAT) affects the patient’s metabolic profile to a lesser degree (Fox et al. 2007; Smith et al. 2012). VAT is considered more metabolically active than SAAT and differs in the secretion of adipokines/cytokines, hormones and immune molecules and in lipolytic/lipogenetic responsiveness, among other things (Bays 2011). Address correspondence to: Loukianos S. Rallidis, 74 Thermopylon Street, Argyroupolis 16451, Athens, Greece. E-mail: rallidis@ath. forthnet.gr Conflicts of Interest: The authors have indicated that they have no conflicts of interest regarding the content of this article. 1083

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Intima-media thickness (IMT) of the carotid arteries measured by B-mode is a well-documented marker of subclinical atherosclerosis (Lorenz et al. 2007). In this study we examined (i) the associations of WC and VAT volume measured by ultrasonography with cardiometabolic risk factors, and (ii) whether VAT is better than WC in the prediction of subclinical carotid atherosclerosis. METHODS Patients One-hundred patients were recruited from the outpatient cardiology department of the University Attikon Hospital and Hygeias Melathron Infirmary in Athens, Greece, between June 2010 and December 2012. They were selected from a pool of 145 healthy employees in a national bank who had been referred for their annual checkup. Exclusion criteria were the presence of diabetes mellitus or CVD (n 5 8), age ,30 y or .70 y (n 5 10), severe obesity (body mass index [BMI] . 35 kg/m2) (n 5 4) and presence of any disease (recent [,2 wk] infection, malignancy or autoimmune disease) that might influence the inflammatory markers (n 5 2). Furthermore, participants were excluded if they had taken part in any weight-reducing program within the last 6 mo or any other nutritional interventions or had engaged in extreme physical activity (.6 h of vigorous exercise per week) (n 5 4). Finally, 17 individuals from the initially selected patients refused to participate in the study. All participants were interviewed, and attention was paid to reporting cardiovascular risk factors and use of medication. The following definitions were used: hypertension, blood pressure (BP) $ 140/90 mmHg and/or anti-hypertensive treatment; hypercholesterolemia, total cholesterol .200 mg/dL and/or lipid-lowering agents; current smoker, a person who smoked at least one cigarette per day until the day of interview. Height, weight and WC were measured. BMI was calculated by dividing weight by height squared (kg/m2). WC was measured by a single experienced cardiologist (L.R.) with the subject standing with the feet close together, at the end of normal expiration with a plastic tape, adjacent to but not compressing the skin, parallel to the floor and to the nearest centimeter, midway between the lowest rib and the iliac crest (Report of the World Health Organization Expert Consultation 2008). The study was approved by the ethics committee of our institution, and all patients gave their informed consent. Blood sampling and laboratory methods Venous blood samples were obtained at 08:00 h after a 12-h overnight fast. Samples were centrifuged using the Labofuge 400R (Heraeus, Germany) at 3000 rpm for

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10 min at 4 C within 2 h of blood collection and were stored at –80 C for further analysis. Serum levels of total cholesterol, high-density lipoprotein (HDL) cholesterol and triglycerides were measured enzymatically on an automatic analyzer (Dimension RXL, Dade Behring, Marburg, Germany). Low-density lipoprotein (LDL) cholesterol was calculated according to Friedewald’s formula: LDL cholesterol 5 total cholesterol - (triglycerides/5 1 HDL cholesterol). Serum levels of apolipoprotein A-1 and apolipoprotein B were measured by immunonephelometry using a BN Prospect analyzer (Dade Behring). High-sensitivity C-reactive protein (hsCRP) was assayed by high-sensitivity particle-enhanced immunonephelometry (N Latex, Dade-Behring) with a range from 0.175 to 1100 mg/L. Finally, glucose levels were measured enzymatically. The intra-assay and interassay coefficients of variation of all measured biochemical parameters were ,5%. Measurements of apolipoproteins and hsCRP were investigational; all other biochemical tests were performed as part of the routine yearly screening. Carotid artery measurements A single cardiologist (L.R.) imaged the common carotid artery intima-media thickness (CCA-IMT) with a 10-MHz linear-array probe using a GE Vivid 7 (Horten, Norway) ultrasound system. The study was performed with the patient supine with the head tilted upward and slightly contralateral to the carotid artery under examination (Aminbakhsh et al. 1999). After the transducer’s depth was optimized, a longitudinal plane of CCA was obtained. CCA-IMT was measured using automated computerized edge tracking software over a uniform length of 10 mm in the far wall of the right and left CCAs within 2 cm proximal to the carotid bulb. Similarly, the far wall of the carotid bulb was also assessed. The program gives the average and also the maximum thickness of the intima-media complex. On each side, three measurements were performed, and for the purpose of the analysis, all measurements were averaged to obtain the mean CCA-IMT. Plaque was defined as a focal wall thickening .50% of the surrounding vessel wall or as a focal thickness .1.5 mm that protrudes into the lumen and is distinct from the adjacent boundary (Stein et al. 2008). All plaques within the common carotids and bulb were recorded. The method had high reproducibility with an intra-observer variability ,8%. Measurement of visceral adipose tissue volume Ultrasonography was performed with a highresolution ultrasonographic system (iU22, Philips, Bothell, WA, USA) as described by Hirooka et al. (2005). Briefly, patients were examined in the supine position. All frozen images were obtained immediately after normal expiration

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Fig. 1. Measurements performed by ultrasonography for the estimation of visceral adipose tissue: (a) Distance between the internal surface of the abdominal muscle and the splenic vein. (b) Distance between the internal surface of the abdominal muscle and the posterior wall of the aorta on the umbilicus. (c) Thickness of the fat layer of the posterior right renal wall in the right posterior perinephric space.

to avoid the influence of respiratory status or abdominal wall tension. The following measurements were performed: (i) the distance between the internal surface of the abdominal muscle and the splenic vein (Fig. 1a), (ii) the distance between the internal surface of the abdominal muscle and the posterior wall of the aorta on the umbilicus (Fig. 1b), (iii) the thickness of the fat layer of the posterior right renal wall in the right posterior perinephric space (Fig. 1c). All parameters were measured with a 3.5-MHz convex-array probe. VAT volume was calculated with the equation: VAT volume 5 –9.008 1 1.191 3 (distance between the internal surface of the abdominal muscle and the splenic vein [mm]) 1 0.987 3 (distance between the internal surface of the abdominal muscle and the posterior wall of the aorta on the umbilicus [mm]) 1 3.644 3 (thickness of the fat layer of the posterior right renal wall [mm]). Statistical analysis Continuous variables are presented as means 6 standard deviations (SD), whereas non-normally distributed variables are presented as medians and interquartile ranges. We used the t-test for independent samples to compare means for normally distributed variables and the Mann-Whitney test for skewed variables. Categorical variables were subjected to the c2 test. The Shapiro-Wilk test for normality was used to evaluate the t-test assumption. Bivariate correlations were performed with Pearson’s correlation coefficient, r. Univariate and multivariate logistic regression was used to analyze associations between the presence of carotid plaques and VAT, WC or BMI. Deviance residuals were used to evaluate the goodnessof-fit of models. Receiver operating characteristic curve analysis and corresponding areas under the curve was used to assess the discriminatory power of VAT and WC on the presence of carotid plaques. A p-value , 0.05 was considered to indicate significance. SPSS Version 21 software (SPSS, Chicago, IL, USA) was used.

RESULTS Baseline characteristics One-hundred patients aged between 30 and 70 y (mean 6 SD 5 49.4 6 8 y) were recruited, of whom 56 had AO defined as WC $ 102 cm for men and WC $ 88 cm for women. The characteristics of the recruited patients with respect to the presence of AO are listed in Table 1. Individuals with AO were older and had higher glucose, uric acid, triglyceride and hsCRP levels and lower HDL cholesterol levels. They had also higher systolic/diastolic BP, greater amounts of VAT and greater CCA-IMTs. Correlations of VAT and WC with clinical and laboratory data The age-adjusted correlations of VAT volume and WC with various cardiometabolic risk factors and CCAIMT are outlined in Table 2. VAT volume was positively and significantly associated with BMI, WC, glucose, triglycerides, uric acid, systolic/diastolic BP, hsCRP and CCA-IMT (Fig. 2) and inversely correlated with HDL cholesterol. WC was also positively correlated with BMI, triglycerides, uric acid, hsCRP and systolic/ diastolic BP and inversely correlated with HDL cholesterol. However, there was no correlation between WC and CCA-IMT or glucose. Association of VAT volume and WC with carotid plaques Logistic regression analysis was performed to assess the association between carotid plaques and VAT, WC and BMI. Univariate logistic regression analysis revealed that VAT volume was associated with the presence of carotid plaques (odds ratio [OR] 5 1.019, 95% confidence interval [CI] 5 1.008–1.030, p 5 0.001). WC was also associated with carotid plaques (OR 5 1.042, 95% CI 5 1.007–1.078, p 5 0.018), but there was no

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Table 1. Baseline characteristics of the study population with respect to the presence of abdominal obesity (AO) based on waist circumference Variable

AO present (n 5 56)

AO not present (n 5 44)

p-value

Sex (male/female) Age (y) Body mass index (kg/m2) Currently smoking (%) Family history of CAD (%) Glucose (mg/dL) Total cholesterol (mg/dL) Triglycerides (mg/dL) HDL cholesterol (mg/dL) LDL cholesterol (mg/dL) Apolipoprotein A-1 (mg/dL) Apolipoprotein B (mg/dL) Uric acid (mg/dL) hsCRP (mg/L) Systolic blood pressure (mm Hg) Diastolic blood pressure (mm Hg) CCA-IMT (mm) Visceral adipose tissue (cm3)

35/21 51.7 6 8.3 31.2 6 3.9 44.6 25.0 97.7 6 11.5 222.3 6 46.8 133.1 6 66.2 47.3 6 10.5 148.4 6 44.9 148.8 6 20.4 109.4 6 25.6 5.13 6 1.4 1.85 (0.94–3.09) 129.7 6 14.9 81.7 6 8.8 0.61 6 0.11 151.9 6 40.5

30/14 46.5 6 6.6 23.9 6 2.9 52.3 22.7 93.3 6 6.6 210.1 6 29.4 101.7 6 56.2 53.9 6 17.3 135.9 6 29.9 150.2 6 29.3 98.9 6 23.9 4.59 6 1.3 1.02 (0.46–2.23) 120.9 6 14.9 77.3 6 10.7 0.56 6 0.12 97.7 6 34.1

0.554 0.001 ,0.001 0.578 0.880 0.037 0.138 0.015 0.020 0.120 0.787 0.051 0.046 0.007 0.005 0.027 0.044 ,0.001

CAD 5 coronary artery disease; CCA-IMT 5 common carotid artery intima-media thickness; HDL 5 high-density lipoprotein; hsCRP 5 high-sensitivity C-reactive protein; LDL 5 low density lipoprotein.

association between BMI and carotid plaques (OR 5 1.082, 95% CI 5 0.993–1.178, p 5 0.072). Multivariate logistic regression analysis revealed that VAT was also an independent predictor of carotid plaques after adjustment for cardiovascular risk factors (i.e., age, gender, hypercholesterolemia, hypertension, smoking and family history of coronary artery disease) (OR 5 1.017, 95% CI 5 1.003–1.031. p 5 0.017). The association persisted after additional adjustment for BMI (OR 5 1.028, 95% CI 5 1.007–1.050, p 5 0.010) or WC (OR 5 1.024, 95% CI 5 1.003–1.031, p 5 0.027), but VAT was no longer a significant predictor after additional adjustment for glucose (OR 5 1.014, 95% CI 5 0.999–1.029, p 5 0.067). Finally, WC was unable to predict, independently of the cardiovascular risk factors, the presence of carotid plaques (OR 5 1.029, 95% CI 5 0.984–1.076, p 5 0.206).

The area under the curve for VAT was 0.719 (95% CI 5 0.617–0.821, p , 0.001), and that for WC was 0.657 (95% CI 5 0.545–0.768, p 5 0.011) as predictors of the presence of carotid plaques. DISCUSSION This is the first study comparing VAT volume measured by an ultrasonographic method with WC with respect to their associations with cardiometabolic risk factors and carotid subclinical atherosclerosis. We found that VAT volume measured by ultrasound according to a method proposed by Hirooka et al. (2005) was associated with cardiometabolic risk factors and CCA-IMT. Additionally, VAT could, independently of the traditional risk factors, predict the presence of carotid plaques, and this remained after adjustment for BMI or WC. On the

Table 2. Age-adjusted Pearson’s correlation coefficients (r) between visceral adipose tissue, waist circumference and clinical and laboratory data Visceral adipose tissue

Waist circumference

Laboratory datum

r

p-value

r

p-value

Body mass index Waist circumference Glucose Total cholesterol Triglycerides High-density lipoprotein cholesterol Uric acid Systolic blood pressure Diastolic blood pressure High-sensitivity C-reactive protein Common carotid artery intima-media thickness

0.760 0.814 0.246 0.084 0.483 –0.516 0.520 0.291 0.233 0.312 0.309

,0.001 ,0.001 0.019 0.413 ,0.001 ,0.001 ,0.001 0.004 0.021 0.002 0.002

0.908 — 0.153 0.087 0.500 –0.519 0.464 0.320 0.273 0.312 0.171

,0.001 — 0.148 0.397 ,0.001 ,0.001 ,0.001 ,0.001 0.007 0.002 0.094

Visceral adipose as predictor of carotid atherosclerosis d L. S. RALLIDIS et al.

Fig. 2. Correlation of visceral adipose tissue (VAT) volume measured by ultrasonography and common carotid artery intima-media thickness (CCA-IMT).

contrary, WC, although associated with most cardiovascular risk factors, was not associated with CCA-IMT and could not, independently of the risk factors, identify the presence of carotid plaques. In our study, WC was positively correlated with BMI, triglycerides, uric acid, systolic/diastolic BP and hsCRP and inversely correlated with HDL cholesterol. The association of WC with cardiometabolic risk factors has been previously reported. Abassi et al. (2013), in a cross-sectional observational study of 492 healthy patients, reported that WC was positively associated with systolic BP, fasting plasma glucose and triglycerides and inversely associated with HDL cholesterol. In another study (Ying et al. 2010) of 1938 young Chinese women, WC was positively associated with systolic BP, diastolic BP and triglycerides and inversely associated with HDL cholesterol. There are only few data regarding the association of WC with subclinical carotid atherosclerosis. Maher et al. (2009) reported an association of WC with carotid IMT in 100 healthy individuals, but this association was abolished when multivariate analysis with cardiovascular risk factors was applied. In another study (Asicioglu et al. 2013), WC was associated with carotid IMT in 50 peritoneal dialysis patients, and the association remained on multivariate analysis. Waist circumference, a simple, inexpensive and reproducible anthropometric marker, has been used as a surrogate measure of VAT. Its association with cardiometabolic risk factors is believed to be due mainly to the adverse metabolic profile of VAT. However, WC provides a measure not only of VAT, but of total abdominal adipose tissue, that is, SAAT and VAT, and it is known that SAAT is approximately twice VAT (Patel and Abate 2013). In

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addition, these two fat depots differ in metabolism and in the secretion of bio-active substances; it has been proposed that SAAT has a more ‘‘benign’’metabolic profile (Porter et al. 2009) or that it might even be ‘‘protective’’ (Britton and Fox 2011). Therefore, the exact contribution of each abdominal fat compartment in the cardiometabolic associations of WC is unknown, and it is possible that the real effect of VAT is underestimated when WC is used as a marker of VAT. Currently, the gold standard for the quantitative measurement of VAT is computed tomography and magnetic resonance imaging (Shuster et al. 2012). Alternatively, ultrasonography is another suitable technique for estimating VAT. We found that VAT volume and WC had the same direction of association with cardiometabolic risk factors; that is, these parameters were positively correlated with BMI, triglycerides, uric acid, systolic/diastolic BP and hsCRP and inversely correlated with HDL cholesterol. However, only VAT was positively correlated with CCA-IMT. A similar association with carotid IMT has previously been reported with other forms of VAT estimates by ultrasonography, such as visceral fat thickness (Kim et al. 2004, 2009). Visceral adipose tissue volume and WC, but not BMI, could predict the presence of carotid plaques in univariate analysis. However, in multivariate logistic analysis, only VAT volume was an independent predictor of carotid plaques after adjustment for traditional cardiovascular risk factors. Given the strong association of VAT volume with WC and BMI and the possibility that VAT is a surrogate for total body fat, we further adjusted our model for BMI or WC. Even after these adjustments, VAT volume remained an independent predictor of carotid plaques. This suggests that the excess risk associated with VAT compared with WC is probably beyond their common cardiometabolic effects. The main limitation of our study is the relatively small number of patients recruited, which precludes subgroup analysis. In addition, insulin resistance, which is a main component of abdominal obesity, was not measured. CONCLUSIONS Although WC provides a simple estimate of AO and is associated with cardiometabolic risk factors, only VAT volume measured by ultrasonography has the advantage of predicting, independently of cardiovascular risk factors, the development of subclinical carotid atherosclerosis. Therefore, VAT volume measured by ultrasonography seems to be a better indicator of early atherosclerotic burden than WC in healthy individuals. Acknowledgments—This study received a grant from the Hellenic Society of Lipidology, Atherosclerosis and Vascular Disease. In addition, the

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authors thank the Echocardiography Department, Attikon Hospital, and Department of Radiology, General Hospital of Nikea, for providing access to their echo machines and facilities.

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Visceral adipose tissue is a better predictor of subclinical carotid atherosclerosis compared with waist circumference.

We investigated whether visceral adipose tissue (VAT) measured by ultrasonography is better than waist circumference (WC) in predicting the presence o...
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