British Journal of Dermatology
C L I N I C A L A N D LA B O R A T O R Y I N V E S T I G A T I O N S
Increased epicardial fat tissue is a marker of subclinical atherosclerosis in patients with psoriasis B. Bulbul Sen,1 N. Atci,2 E.N. Rifaioglu,1 O. Ekiz,1 I. Kartal,2 E. Buyukkaya,3 M. Kurt,3 M.F. Karakas,3 S. Buyukkaya,4 A.B. Akcay3 and N. Sen3 Departments of 1Dermatology 2Radiology and 3Cardiology, Mustafa Kemal University School of Medicine, Hatay, Turkey 4 Department of Cardiology, Antakya State Hospital, Hatay, Turkey
Summary Correspondence Bilge Bulbul Sen. E-mail: [email protected]
Accepted for publication 29 July 2013
Funding sources None.
Conflicts of interest None declared. DOI 10.1111/bjd.12569
Background Carotid intima–media thickness (CIMT) is a potential indicator of subclinical atherosclerosis in patients with psoriasis. Epicardial fat thickness (EFT) is proposed as a new cardiometabolic risk factor. Objective To evaluate the association between EFT and CIMT in patients with psoriasis. Methods This was a cross-sectional and observational study; 65 patients with psoriasis and 50 age- and sex- matched control subjects were included. Data about echocardiographic EFT, CIMT, anthropometric measurements and metabolic profile were obtained. Results The EFT and CIMT were significantly increased (73 05 vs. 65 05 mm, P < 001; 074 011 vs. 060 007 mm, P < 001, respectively) in patients with psoriasis compared with the controls. EFT was significantly correlated with CIMT (r = 069, P < 001). In a multiple linear regression model in which EFT was independently associated with psoriasis (b = 045, P < 001), age (b = 033, P = 001), CIMT (b = 050, P < 001), body mass index (b = 025, P = 001), high-sensitivity C-reactive protein (b = 032, P < 001) and duration of disease (b = 034, P = 003). Conclusions We demonstrated that EFT and CIMT are increased in patients with psoriasis, and that echocardiographic EFT is closely correlated with CIMT in patients with psoriasis. The echocardiographic assessment of EFT may have the potential to be a simple marker of subclinical atherosclerosis and increased cardiovascular risk in patients with psoriasis.
What’s already known about this topic?
The risk of myocardial infarction, stroke and cardiovascular mortality increases in patients with psoriasis. Carotid intima–media thickness (CIMT) is a potential indicator of subclinical atherosclerosis in patients with psoriasis. Epicardial fat thickness (EFT) is proposed as a new cardiometabolic risk factor.
What does this study add?
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© 2013 British Association of Dermatologists
EFT and CIMT are increased in patients with psoriasis compared with healthy controls. Echocardiographic EFT is closely correlated with CIMT in patients with psoriasis. The echocardiographic assessment of EFT may have the potential to be a simple marker of subclinical atherosclerosis and increased cardiovascular risk in patients with psoriasis.
British Journal of Dermatology (2013) 169, pp1081–1086
1082 Epicardial fat tissue and psoriasis, B. Bulbul Sen et al.
Psoriasis is a chronic, immune-mediated, inflammatory disorder affecting 15–3% of the general population.1 The exact mechanism of the disease remains unknown. Various cardiovascular conditions may accompany psoriasis due to the accelerated atherosclerosis.2,3 The risk of developing cardiovascular risk factors and the risk of myocardial infarction, stroke and cardiovascular mortality increases particularly in subjects with severe psoriasis.4–6 Carotid intima–media thickness (CIMT) and plaque frequency are established risk markers of subclinical atherosclerosis predicting myocardial infarction and stroke development.7 Previous studies have shown that patients with psoriasis exhibit greater CIMT than controls.8–10 Epicardial adipose tissue is a component of visceral adipose tissue located around the heart between myocardial and visceral epicardium. This metabolically active tissue releases various bioactive molecules.11 Previous studies have demonstrated the association between epicardial adipose tissue and insulin resistance,12 diabetes mellitus,13 increased cardiometabolic risk,14 inflammatory markers15,16 and coronary artery disease (CAD).17 Furthermore, some studies have shown an association between CIMT or carotid plaque and epicardial fat thickness (EFT).18,19 However, no studies have been performed on the association between EFT and psoriasis. The objective of this study was to evaluate whether echocardiographic EFT indicates CIMT in patients with psoriasis.
ethics committee and all individuals gave written informed consent. The study was also carried out according to the recommendations set forth by the Helsinki Declaration on biomedical research involving human subjects. Measurement of epicardial fat thickness Transthoracic echocardiography was performed in all participants in the left lateral position according to the American Society of Echocardiography guidelines using the GE-Vivid 7 system (GE-Vingmed Ultrasound AS, Horten, Norway). Echocardiography was done by a cardiologist who had substantial specialty in echocardiography and who was unaware of the clinical data. All data were transmitted to a workstation for further analysis (EchoPAC 6.1; GE Vingmed Ultrasound AS). The EFT was measured on the free wall of the right ventricle from the parasternal long-axis view (Fig. 1), as previously described and validated.20 EFT was described as an echo-free space in the pericardial layers on the two dimensional echocardiography, and its thickness was measured perpendicularly on the free wall of the right ventricle at end-systole for three to 10 cardiac cycles. The measurement was performed at a point on the free wall of the right ventricle along the midline of the ultrasound beam, perpendicular to the aortic annulus. In order to increase the confidence in the results, EFT measurement was performed at two different moments and the percentage of R-R interval with the least amount of motion was used.
Patients and methods Measurement of carotid intima–media thickness Study population The study population included 65 consecutive patients with psoriasis vulgaris who were referred from our Department of Dermatology (39 men; mean age 411 33 years, mean disease duration 116 42 years) and 50 healthy subjects as controls (28 men; mean age 405 38 years). The diagnosis of psoriasis was based on a clinical or histopathological examination of all patients. Age, sex, duration of the disease, smoking habits of the patients, body mass index (BMI), waist circumference and admission biochemical measurements [fasting blood glucose, high-sensitivity C-reactive protein (hs-CRP), total cholesterol, high-density lipoprotein (HDL) cholesterol, lowdensity lipoprotein (LDL) cholesterol and triglyceride levels] were recorded. BMI was calculated as the ratio of weight (kg) to height (m) squared (kg m 2). The control subjects had no cardiovascular or any other organ system disease. None of the patients had hypertension (systolic blood pressure > 140 mmHg or diastolic blood pressure > 90 mmHg), renal failure (serum creatinine values > 13 mg dL 1), diabetes mellitus (fasting overnight venous plasma concentration > 110 mg dL 1), cancer, infectious diseases, left ventricle ejection fraction < 50%, moderate or severe valvular stenosis and/or regurgitation, CAD or chronic obstructive pulmonary disease, or were pregnant. The patients with poor echocardiographic image quality were also excluded. The study was reviewed and approved by the local British Journal of Dermatology (2013) 169, pp1081–1086
Carotid intima–media thickness was measured by recording ultrasonographic images of both the left and the right common carotid arteries with a 75-MHz linear array transducer (Vivid 7 dimension; General Electric Medical Systems, Horten, Norway). The transducer was manipulated so that the near and far walls of the common carotid artery were parallel to the transducer footprint, and the lumen diameter was maximized in the longitudinal plane. A region 1 cm proximal
Fig 1. Measurement of epicardial fat thickness (EFT) by twodimensional echocardiography on the parasternal long-axis image. LA, left atrium; AO, aorta; RVOT, right ventricular outflow tract. © 2013 British Association of Dermatologists
Epicardial fat tissue and psoriasis, B. Bulbul Sen et al. 1083
to the carotid bifurcation was identified, and the intima– media thickness of the far wall was evaluated as the distance between the lumen–intima interface and the media–adventitia interface. The intima–media thickness measurement was obtained from four contiguous sites at 1-mm intervals, and the average of the four measurements was used for analyses. After the measurements were taken from both the right and left common carotid arteries, the average of the two values was calculated. All measurements were made manually on still images obtained during the sonographic scanning. A plaque was defined as a localized thickening of at least 12 mm that did not uniformly involve the artery. The intraobserver variability of ultrasonographic measurements was < 4% and all examinations were performed by a single experienced examiner who was blinded to the clinical and biochemical data. Evaluation of psoriasis severity The clinical severity of psoriasis was evaluated using the Psoriasis Area and Severity Index (PASI) score.21 Statistical analyses Statistical analyses were performed using SPSS software package program (IBM, New York, NY, U.S.A.), version 17.0 for Windows. After certification of normal distribution, data were reported as mean SD; categorical variables were defined as percentage. An independent sample t-test or Mann–Whitney U-test was used to compare the study variables between psoriasis patients and control subjects. For categorical variables the v2 test was used. Multivariate linear regression analysis was used to evaluate the correlates of EFT. In a multiple regression model in which EFT was included as a dependent variable together with psoriasis, age, male sex, CIMT, blood pressure, BMI, waist circumference, fasting glucose level, cholesterol levels, triglyceride, hs-CRP, PASI score and duration of disease. The linear regression model included the variables that were significant (P < 01) in the univariate analyses. Statistical significance was defined as P < 005.
Results Characteristics of the study groups are displayed in Table 1. The two groups were similar in terms of age, sex, smoking status, waist circumference, BMI, blood pressure, fasting glucose, creatinine and cholesterol levels (Table 1). In the psoriasis group, the mean hs-CRP values were significantly higher, compared with the controls (210 113 vs. 119 071 mg L 1, P < 001). The EFT and CIMT were significantly increased (73 05 vs. 65 05 mm; P < 001; 074 011 vs. 060 007 mm; P < 001, respectively) in patients with psoriasis compared with the controls (Fig. 2). EFT was significantly correlated with CIMT (r = 069, P < 001) (Fig. 3). Table 2 shows the correlation of EFT with other clinical variables. © 2013 British Association of Dermatologists
Table 1 Demographic, clinical and laboratory features of the subjects
Age (years) Sex (F/M), n Smoking, n (%) Height (cm) Weight (kg) Waist circumference (cm) Body mass index (kg m 2) Fasting glucose (mg dL 1) SBP (mmhg) DBP (mmhg) Creatinine (mg dL 1) Total cholesterol (mg dL 1) LDL-cholesterol (mg dL 1) HDL-cholesterol (mg dL 1) Plasma triglyceride (mg dL 1) hs-CRP (mg L 1) PASI score Disease duration (years) Topical steroid, calcipotriol, n (%) Methotrexate, n (%) Ciclosporin, n (%) Phototherapy, n (%) Acitretin, n (%) CIMT (mm) Epicardial fat thickness (mm)
Patients with psoriasis, n = 65
Healthy controls, n = 50
411 33 26/39 17 (26) 169 5 75 9 92 14 259 28 85 160 105 8 75 7 099 028 190 46
405 38 22/28 15 (30) 170 6 74 8 94 13 255 23 87 13 103 10 78 10 094 021 199 37
03 040 041 032 091 089 039 039 032 014 041 037
060 007 65 05
< 001 < 001
210 175 116 18
113 57 42 (28)
15 13 10 9 074 73
(23) (20) (15) (14) 011 05
Values are mean SD unless otherwise indicated. SBP, systolic blood pressure; DBP, diastolic blood pressure; HDL, high-density lipoprotein; LDL, low-density lipoprotein; PASI, Psoriasis Area and Severity Index; hs-CRP, high-sensitivity C-reactive protein; CIMT, carotid intima–media thickness.
In a multiple regression model in which EFT was included as a dependent variable together with psoriasis, age, male sex, CIMT, blood pressure, BMI, waist circumference, fasting glucose level, cholesterol levels, triglyceride, hs-CRP, PASI score and duration of disease, the EFT was independently associated with psoriasis (b = 045, P < 001), age (b = 033, P = 001), CIMT (b = 050, P < 001), BMI (b = 025, P = 001), hs-CRP (b = 032, P < 001) and duration of disease (b = 034, P = 003) (Fig. 3).
Discussion In our study, we have demonstrated two main results: firstly, EFT and CIMT are increased in patients with psoriasis compared with healthy controls, reflecting subclinical atherosclerosis; and, secondly, echocardiographic EFT is closely correlated with CIMT in patients with psoriasis. British Journal of Dermatology (2013) 169, pp1081–1086
1084 Epicardial fat tissue and psoriasis, B. Bulbul Sen et al.
(a) Carotid intima–media thickness (mm)
Epicardial fat thickness (mm)
P < 0·001 8·00
(a) Carotid intima–media thickness (mm)
r = 0·42 P < 0·01
30 6.00 7.00 8.00 Epicardial fat thickness (mm)
r = 0·69 P < 0·01
r = 0·28 P < 0·01
6.00 7.00 8.00 Epicardial fat thickness (mm)
r = 0·31 P < 0·01
28.00 Hs-CRP (mg/L)
Body mass index, kg/m2
Fig 2. Comparison of (a) epicardial fat thickness and (b) carotid intima–media thickness between patients with psoriasis and the control group.
45 Age (years)
P < 0·001
0·40 Control group
6.00 7.00 8.00 Epicardial fat thickness (mm)
6.00 7.00 8.00 Epicardial fat thickness (mm)
Psoriasis is associated with increased vascular inflammation22 and atherosclerotic vascular disease.23,24 The atherosclerotic process starts during childhood.25 It is important to determine preclinical atherosclerosis in order to take necessary precautions prior to development of vascular events; noninvasive tests have been developed for the early detection of atherosclerosis for this reason. One of these methods is measuring CIMT using high-resolution ultrasonography. An absolute CIMT difference of 01 mm increases the risk of myocardial infarction by 10–15% and the risk of stroke by 13–18%.7 Previous studies showed that patients with psoriasis exhibit greater CIMT than controls.8–10 In our study, in accordance with the literature, CIMT was higher in patients with psoriasis than the control group. The potential association between psoriasis and increased CIMT may be related to persistent inflammation.26 Visceral adipose tissue is considered to be a metabolically active endocrine and paracrine organ releasing proinflammatory and proatherogenic cytokines. Epicardial adipose tissue is a type of ectopic visceral adipose tissue. It is derived from the same embryological origin with intra-abdominal visceral British Journal of Dermatology (2013) 169, pp1081–1086
Fig 3. Correlation between epicardial fat thickness and (a) age, (b) carotid intima– media thickness, (c) body mass index and (d) high-sensitivity C-reactive protein (hs-CRP).
adipose tissue.27 Similar to other visceral adipose tissues, epicardial adipose tissue functions as a lipid store that secretes hormones, inflammatory cytokines and chemokines [such as tumour necrosis factor (TNF)-a, monocyte chemoattractant protein (MCP)-1, interleukin (IL)-6 and plasminogen activator inhibitor-1].28 Previous studies demonstrated the association between EFT and CAD,29 coronary calcium score,28 insulin resistance,19,30 diabetes mellitus13 and metabolic syndrome.12 There are also studies showing the association between EFT and the markers of subclinical atherosclerosis, such as CIMT or carotid plaque.18,19,31 There are various findings proving the contribution of epicardial adipose tissue in the pathogenesis of CAD. Firstly, postautopsy EFT correlates with the propagation of CAD.32 Another proof is the paracrine effect of epicardial adipose tissue leading to the release of inflammatory cytokines affecting coronary arteries.11 Furthermore, epicardial adipose tissue releases higher levels of proatherogenic IL-6 mRNA in subjects with CAD compared with those without CAD.33 The present study demonstrated higher EFT and CIMT values in patients with psoriasis compared with the control group. In addition, © 2013 British Association of Dermatologists
Epicardial fat tissue and psoriasis, B. Bulbul Sen et al. 1085 Table 2 Independent predictors for epicardial fat tissue by multivariate linear regression analysis Univariate analysis
Psoriasis Age Male sex CIMT Systolic blood pressure Diastolic blood pressure Body mass index Waist circumference Fasting glucose Total cholesterol LDL-cholesterol HDL-cholesterol Triglyceride hs-CRP PASI score Duration of disease
054 042 021 069 028 023 028 030 034 024 030 019 021 031 032 036
< 001 < 001 032 < 001 002 015 < 001 001 001 011 < 001 018 022 < 001 012 < 001
< 001 001
025 027 028
001 004 021
CIMT, carotid intima–media thickness; LDL, low-density lipoprotein; HDL, high-density lipoprotein; hs-CRP, high-sensitivity C-reactive protein; PASI, Psoriasis Area and Severity Index.
even after controlling for BMI, waist circumference, LDL levels, hs-CRP and duration of disease, psoriasis as an independent risk factor is still associated with increased CIMT and EFT. The association between psoriasis and atherosclerotic disease has not been fully clarified. The increased prevalence of cardiovascular risk factors may be contributing to the accelerated atherosclerosis in patients with psoriasis,34 or the systemic and persistent inflammation related to the continuous release of TNF-a and other proinflammatory cytokines may be playing a major role in the increased cardiovascular risk.35 Why is the EFT increased in patients with psoriasis? One of the possible mechanisms may be the persistent inflammation. The precursor inflammatory adipokines (such as TNF-a, MCP1, IL-6, etc.) are known to induce persistent inflammation and potentially to cause predisposition to atherosclerosis. Also, patients with psoriasis exhibit increased incidence of diabetes mellitus, hypertension, metabolic syndrome and dyslipidaemia;36,37 these comorbidities may be contributing to the increased EFT. Furthermore, increased EFT in patients might be related to the physiopathogenetic basis of psoriasis, which causes increased risk in cardiovascular disease. We believe that identifying a relationship between psoriasis and increased EFT can provide new insights into the association between psoriasis and atherosclerosis. In our study, EFT was associated with duration of disease but it was not associated with PASI. In patients with longer duration of disease, the number of flares and cumulative effect of chronic inflammation might be higher and thus inflammatory damage and the risk of cardiovascular disease might be © 2013 British Association of Dermatologists
increased. However, the PASI score shows the current clinical severity of the disease. One-time measurement of PASI may not be sufficient to predict the long-term prognosis of the disease and comorbidities. That may be why EFT does not correlate with the disease severity. There was no difference regarding blood glucose, blood pressure, metabolic syndrome and dyslipidaemia across the groups in the present study. As a result, the increased EFT in patients with psoriasis in our study and the association between EFT and CIMT and hs-CRP indicate that EFT may be used as a marker of subclinical atherosclerosis in patients with psoriasis. EFT can be measured easily during routine echocardiographic examination and may be used for the diagnosis of subclinical atherosclerosis and provide benefits regarding further diagnostic studies, aggressive lifestyle changes and selection of patients for primary preventive treatment. Our study presents some limitations. Firstly, the inclusion criteria of this study were strict. Therefore, the results of the present study may not be applicable to patients in the general population. Secondly, an important limitation of the study was the small sample size. The third limitation is the crosssectional design of the study; the study groups were not under clinical follow-up and it may not be possible to evaluate fully the reason underlying the association between the covariates. To clarify this point, a prospective study involving clinical intervention will be needed. The fourth limitation is the fact that the gold standard in assessing EFT is magnetic resonance imaging (MRI); the lack of MRI use is one of the limitations of the present study. While MRI and computed tomography readily evaluate EFT, these methods are not always easily accessible and applicable. Although EFT by echocardiography has inherent errors compared with computed tomography and MRI, echocardiography is an objective, noninvasive and readily available method, and is less costly. Lastly, insulin resistance was not evaluated in our study. In conclusion, we demonstrated that EFT and CIMT are increased in patients with psoriasis compared with healthy controls, and that echocardiographic EFT is closely correlated with CIMT in patients with psoriasis. The echocardiographic assessment of EFT may have the potential to be a simple marker of subclinical atherosclerosis and increased cardiovascular risk in patients with psoriasis.
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