Download Increased Amount of Visceral Fat in Patients with Psoriasis

Original Paper
Dermatology 2010;220:32–37
DOI: 10.1159/000254482
Received: May 28, 2009
Accepted after revision: August 4, 2009
Published online: October 29, 2009
Increased Amount of Visceral Fat in
Patients with Psoriasis Contributes to
Metabolic Syndrome
Ali Balci a Didem Didar Balci b Zafer Yonden c Inan Korkmaz a
Julide Zehra Yenin b Ebru Celik b Nese Okumus c Ertugrul Egilmez a
Departments of a Radiology, b Dermatology and c Biochemistry, Faculty of Medicine, Mustafa Kemal University,
Antakya, Turkey
Key Words
Psoriasis ⴢ Visceral fat ⴢ Metabolic syndrome
Abstract
Background: Psoriasis is associated with obesity and metabolic syndrome. Metabolic syndrome is associated with visceral fat accumulation. There is no study on the accumulation of visceral fat in patients with psoriasis. Objective: The
aim of this study was to compare the visceral fat accumulation in patients with psoriasis and controls. Subjects and
Methods: 46 patients with psoriasis and 46 sex- and agematched control patients were included in this study. The
abdominal fat area [visceral fat area (VFA), subcutaneous fat
area (SFA) and total fat area (TFA)] at the level of the umbilicus was evaluated by computed tomography. Results: The
mean VFA value and VFA/SFA ratio of the psoriasis patients
were significantly higher compared with the control patients
(123.4 8 80.3 vs. 81.2 8 59.8 cm2 and 0.734 8 0.593 vs. 0.491
8 0.336; p = 0.005 and p = 0.017, respectively). Fasting blood
sugar levels were also found to be significantly higher in psoriasis patients, compared with the control patients (101.8 8
43.5 vs. 83.4 8 9.1 mg/dl; p = 0.005). Multiple linear regression analysis indicated that waist-to-hip ratio, age, body
weight, the presence of psoriasis and metabolic syndrome
were significantly associated with VFA. Conclusion: Psoriasis
patients had a higher amount of VFA, compared with the
control patients.
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Introduction
Psoriasis is a systemic, chronic, inflammatory skin
disease that affects approximately 2% of the population
[1]. Recently, associations have been recognized between
psoriasis and an increased incidence of atherosclerotic
diseases and metabolic syndrome (central obesity, diabetes or insulin resistance, hypertension, and dyslipidaemia) [2–5].
Abdominal obesity, which is caused by excess accumulation of visceral adipose tissue (VAT), is associated
with increased risk for cardiovascular disease and diabetes mellitus [6, 7]. The visceral component of abdominal
fat is the most prevalent form in insulin resistance and
metabolic syndrome [8]. Studies have clearly shown that
viscerally obese patients have the most disturbed metabolic risk profile. An excess and disproportionate accumulation of VAT is responsible for metabolic and atherosclerotic diseases more frequently than the excess accumulation of subcutaneous or total body fat [6–9]. The
accumulation of VAT is a risk factor for carotid and coronary atherosclerosis, irrespective of body weight [10, 11].
Anthropometric measurements such as the waist-to-hip
ratio (WHR) and sagittal abdominal diameter are simple
and useful indicators of VAT accumulation, but these indices do not always accurately reflect visceral adiposity
[12–14]. Computed tomography (CT) is an optimal, reproducible, and reliable technique for accurately assess-
Didem Didar Balci
Department of Dermatology, Faculty of Medicine
Mustafa Kemal University
TR–31100 Antakya (Turkey)
Tel. +90 326 214 0649, Fax +90 326 214 4977, E-Mail didemaltiner @ yahoo.com
ing visceral fat accumulation. Using CT, visceral and subcutaneous fat can be accurately quantified, with small
intra- and interobserver variation, allowing the determination of their relationships with biochemical and anthropometric measurements [15, 16].
This study is the first to determine visceral fat accumulation in psoriasis patients compared with controls.
We also investigated the association of visceral fat accumulation with metabolic syndrome and anthropometric
measurements in patients with psoriasis.
Subjects and Methods
Study Patients
46 consecutive patients with psoriasis vulgaris and 46 genderand age-matched control patients attending our dermatology outpatient clinic were included in this study. Informed consent was
obtained from all patients, and the study protocol was approved
by the ethics committee of our institution. The diagnosis of psoriasis vulgaris was based on a clinical or histopathological examination of all patients. Controls were recruited among the patients
referred for dermatological conditions other than psoriasis. The
diagnoses of the controls were skin neoplasm (5 patients, 10.9%:
e.g. squamous cell carcinoma, basal cell carcinoma), superficial
fungal infections (17 patients, 37.0%), contact dermatitis (8 patients, 17.4%), lichen planus (3 patients, 7.0%), vitiligo (4 patients,
8.7%), and urticaria (9 patients, 20.0%). The psoriasis and control
patients were of the same ethnic origin. A known endocrine, kidney, or metabolic disease other than obesity or diabetes mellitus
and age younger than 18 years were exclusion criteria. Subjects
who were receiving lipid-lowering therapy were also excluded
from the study.
Before conducting the study, a power analysis was performed
based on the results of a pilot study (n = 20). Using a sample size
calculator (DSS Research, Fort Worth, Tex., USA), it was estimated that 43 subjects for each group were needed to give this study
a power of 90% for showing a relevant change in visceral fat area
(VFA) with a 95% confidence interval.
Anthropometric characteristics, including age, gender, weight,
height, body mass index (BMI), and WHR, and clinical characteristics, including duration of disease, type and severity of disease, medications, blood pressure, and smoking habits, were recorded. The WHR was calculated as the ratio of the waist and hip
circumferences. BMI was calculated as the ratio of the weight (kg)
to the square of the height (m) (kg/m2). Morning blood pressure
was measured using a mercury sphygmomanometer, after a 15min rest with the patient in the sitting position. Blood pressure
was recorded as the average of two consecutive measurements.
Disease severity was quantified using the Psoriasis Area and Severity Index (PASI).
Laboratory Measurements
To measure serum total cholesterol, high-density lipoprotein
(HDL) cholesterol, low-density lipoprotein (LDL) cholesterol, triglyceride, uric acid, and glucose levels, blood samples were obtained in the morning after an overnight fast of at least 8 h. Serum
Increased Visceral Fat in Psoriasis
total cholesterol, HDL and LDL cholesterol, triglyceride, uric
acid, and glucose levels were determined spectrophotometrically
using an autoanalyser (Synchron LX20; Beckman Coulter, Fullerton, Calif., USA). To diagnose diabetes mellitus, subjects who
had a fasting blood sugar in the range of 110–126 mg/dl underwent a standard (75 g glucose) oral glucose tolerance test, as proposed by the World Health Organization, between 8 and 11 a.m.
[17]. The number of diagnostic criteria for metabolic syndrome in
each study subject was recorded. The criteria of the National Cholesterol Education Program’s Adult Panel III for metabolic syndrome were used: waist circumference 1102 cm in men or 188 cm
in women; hypertriglyceridaemia 1150 mg/dl; HDL cholesterol
!40 mg/dl in men or !50 mg/dl in women; blood pressure 1130/85
mm Hg or antihypertensive medication; fasting plasma glucose
1110 mg/dl or known diabetes mellitus. Subjects who had three
or more criteria were diagnosed with metabolic syndrome [18].
Measurement of Abdominal Fat Distribution
Abdominal fat distribution was examined on one cross-sectional CT (Toshiba Aquilion 64 scanner, Tokyo, Japan) scan (120
kV, 200 mA, 5-mm section thickness) at the level of the umbilicus
(fourth lumbar vertebra) with the patient in the supine position,
using a previously described procedure [16]. A region of interest
in the subcutaneous fat layer was defined by tracing its contour
on each scan, and the attenuation range of CT numbers for fat tissue was calculated and expressed as the mean 8 2 standard deviations (SD). Intraperitoneal tissue was defined by tracing its
contour on each scan; within that region of interest, tissue with
attenuation within the attenuation mean 8 2 SD for fat tissue was
considered VFA (fig. 1). VFA was measured as the fat tissues located in the intraperitoneal, omental, and retroperitoneal areas.
Total abdominal tissue with attenuation within the mean 8 2 SD
for fat tissue was considered as the total fat area (TFA) (fig. 2). The
subcutaneous fat area (SFA) was calculated as TFA minus VFA.
The measurements were extrapolated by one of the authors (I.K.),
using a previously described procedure [16]. The subjects had fasted overnight and were studied in the morning, between 8 and 12
a.m. All laboratory parameters and anthropometric measurements were obtained on the same day as the CT examination.
Statistical Analysis
Continuous data are expressed as the mean 8 SD, and categorical variables are expressed as percentages. The normality of
the variables was tested using the Kolmogorov-Smirnov test.
Comparisons between two groups were assessed using Student’s
t test for continuous variables and a ␹2 test for categorical variables. The Mann-Whitney U test was used for continuous variables that were not distributed normally. Correlations between
variables were analyzed using the Pearson correlation analysis.
Multiple linear regression analysis was used to assess independent associations between VFA and other variables. The variables
significantly associated with VFA (p ! 0.05) in the Pearson correlation analysis were included as independent variables in multiple linear regression analysis models. A stepwise selection method was used in the multiple linear regression analysis. Two-sided
p values of less than 0.05 were considered statistically significant.
The statistical analysis was carried out using the Statistical Package for the Social Sciences (SPSS) version 16 (SPSS, Chicago, Ill.,
USA).
Dermatology 2010;220:32–37
33
Fig. 1. A CT scan obtained at the level of the umbilicus. The area
in pink is regarded as VFA.
Fig. 2. A CT scan obtained at the level of the umbilicus. The area
in pink shows TFA.
Results
34
Dermatology 2010;220:32–37
400
300
VFA
The main demographic, clinical, and laboratory features of the subjects are shown in table 1. The two groups
were comparable in terms of age, gender, BMI, WHR, total cholesterol, LDL cholesterol, HDL cholesterol, triglyceride, uric acid levels, TFA, and SFA. However, the mean
VFA and VFA/SFA ratio of the psoriasis patients were
significantly higher than those in the control patients
(123.4 8 80.3 vs. 81.2 8 59.8 cm2 and 0.734 8 0.593 vs.
0.491 8 0.336; p = 0.005 and p = 0.017, respectively)
(fig. 3). The fasting blood sugar level was also significantly higher in the psoriasis patients than in the controls
(101.8 8 43.5 vs. 83.4 8 9.1 mg/dl; p = 0.005).
The presence of diabetes mellitus and smoking habit
were significantly more frequent in psoriasis patients
compared with controls. However, the prevalence of hypertension did not differ significantly between the two
groups (table 1).
Table 2 shows the results of multiple linear regression
analyses for factors associated with VFA in the entire
group of 92 study subjects and in the psoriasis patients
only. Multiple linear regression analysis in all study subjects indicated that VFA was significantly associated with
WHR, age, body weight, presence of psoriasis, and metabolic syndrome. Multiple linear regression analyses of
the factors associated with VFA in psoriasis patients only
indicated that VFA was significantly associated with
WHR, age, body weight, and presence of metabolic syn-
44
2
200
100
0
Controls
(n = 46)
Patients
(n = 46)
Fig. 3. Boxplot graph of VFA in patients with psoriasis and controls. The upper and lower sides of each box show the upper and
lower quartile, respectively, while the horizontal line dividing
each box shows the median. Circles represent outliers.
drome (table 2). BMI was not associated with VFA in the
linear regression analysis.
PASI score, duration or type of disease, smoking habit, and therapies were not associated with VFA (p 1 0.05).
None of the laboratory findings were associated with
VFA (p 1 0.05). At the time of the study, 22 (47.8%) patients were using topical corticoid or calcipotriol; 4 (8.7%)
acitretin, 2 each (4.3% each) phototherapy and biologics,
Balci /Balci /Yonden /Korkmaz /Yenin /
Celik /Okumus /Egilmez
Table 1. Demographic, clinical and laboratory features of the subjects
Psoriasis patients (n = 46)
Age, years
Male/female
Disease duration, years
PASI score
BMI, kg/m2
WHR, %
Total cholesterol, mg/dl
LDL cholesterol, mg/dl
HDL cholesterol, mg/dl
Triglyceride, mg/dl
Fasting blood sugar, mg/dl
Uric acid, mg/dl
Smoking
Diabetes mellitus
Hypertension
Metabolic syndrome
VFA, cm2
TFA, cm2
SFA, cm2
VFA/SFA, %
39.5814.2
29/17
11.088.3
6.186.3
26.584.2
90.688.3
178.8836.6
107.8834.4
43.6810.5
139.78129.9
101.8843.5
4.481.3
24 (52.2)
7 (15.2)
4 (8.7)
8 (17.4)
123.4880.3
291.88148.7
168.4891.3
73.4859.3
Controls (n = 46)
p values
39.8813.5
29/17
0.898a
1
26.884.1
88.187.5
170.1839.0
103.4835.6
42.1811.6
119.1874.2
83.489.1
4.681.0
14 (30.4)
1 (2.2)
5 (10.9)
5 (10.9)
81.2859.8
268.08126.0
186.8893.4
49.1833.6
0.760a
0.132a
0.310a
0.542a
0.516a
0.631b
0.005b
0.419a
0.028c
0.029c
0.500c
0.275c
0.005a
0.410a
0.342a
0.017a
Figures in parentheses are percentages. a Student’s t test. b Mann-Whitney U test. c ␹2 test.
and 1 each (2.2% each) cyclosporine, methotrexate, and
salazopyrine. The remaining 13 (28.3%) were not taking
any therapy. 40 (87.0%) of the psoriasis patients had the
plaque type, 5 (10.9%) had the guttate type, and the remaining 1 (2.2%) had the erythrodermic type. 3 (6.5%)
patients had psoriatic arthritis.
This study clearly demonstrated for the first time that
VFA is increased in psoriasis patients compared with
control patients with similar waist circumferences. This
study also clarified that VFA is independently associated
with the presence of metabolic syndrome in patients with
psoriasis. Several recent studies have indicated that psoriasis patients tend to develop metabolic syndrome, which
is a cluster of conditions that include increased waist circumference, dyslipidaemia, hypertension, and diabetes
mellitus or insulin resistance [2–5]. Other comorbidities
such as smoking habit and obesity have also been reported more frequently in patients with psoriasis than in nonpsoriatic controls [19, 20]. In the present study, diabetes
mellitus and smoking habit were more common in pso-
riatic patients than in controls, whereas no significant
difference was found in the prevalence of hypertension or
metabolic syndrome between psoriasis patients and controls. However, this study did not aim to compare the
prevalence of these comorbidities, and the study population was too small for an analysis of these parameters.
Obesity may be accompanied by several metabolic disturbances, including diabetes mellitus, dyslipidaemia,
insulin resistance, and atherosclerotic diseases. In general, the risk associated with obesity is proportional to the
total amount of excess adipose tissue, but visceral obesity
appears to be an important indicator of metabolic and
atherosclerotic diseases [6–9]. In psoriasis, the chronic
inflammation and persistent secretion of TNF-␣ and
other pro-inflammatory cytokines together with comorbidities such as metabolic syndrome and smoking habit
appear to be the main cause of increased atherosclerosis
[2, 3, 19, 20].
A number of mechanisms have been proposed to explain the association between visceral adiposity and metabolic complications and atherosclerosis. First, visceral
fat, owing to its anatomical location and peculiar metabolism (enhanced lipolytic activity), releases toxic free fatty acids (FFAs), which are delivered in high concentration
Increased Visceral Fat in Psoriasis
Dermatology 2010;220:32–37
Discussion
35
Table 2. Multiple linear regression analysis factors associated with VFA in the entire group and psoriasis
patients only
Independent variables
WHR
Age
Body weight
Presence of metabolic syndrome
Presence of psoriasis
R2 (multiple coefficient of determination)
Standard regression coefficients (␤)
VFA in psoriasis
patients only (n = 46)
VFA in all study
subjects (n = 92)
0.412***
0.282**
0.219*
0.245**
–
0.787***
0.343***
0.293***
0.278***
0.182**
0.222***
0.773***
* p < 0.05; ** p < 0.01; *** p < 0.001.
VFA is significantly associated with WHR (p < 0.001), age (p < 0.01), body weight (p < 0.05) and presence of
metabolic syndrome (p < 0.01) in psoriasis patients only. VFA is significantly associated with WHR (p < 0.001),
age (p < 0.001), body weight (p < 0.001), presence of metabolic syndrome (p < 0.01) and presence of psoriasis
(p < 0.001) in all study subjects.
to the liver. An excessive accumulation of FFAs in the
liver impairs hepatic insulin sensitivity, resulting in peripheral hyperinsulinaemia and insulin resistance [8, 21,
22]. In addition, an increased amount of FFAs in the liver
is ultimately responsible for the production of highly atherogenic small dense LDLs [8]. Second, adipose tissue
functions as an endocrine organ, releasing pro-inflammatory and adipocyte-derived cytokines such as TNF-␣,
leptin, resistin, and adiponectin, which are thought to
constitute an important link between obesity and insulin
resistance [8, 20, 23, 24]. These cytokines can also contribute to an increased risk for atherosclerotic diseases
[8]. More recently, Takahashi et al. [25] reported that
plasma adiponectin levels were decreased and plasma
leptin levels increased in psoriasis patients compared
with healthy controls. In that study, a negative correlation
was also demonstrated between plasma adiponectin levels and both the PASI score and TNF- ␣ level in psoriasis
patients. Adiponectin is the most abundant adipocytespecific adipokine in the circulation. This important cytokine has anti-inflammatory effects and functions in
regulating insulin sensitivity [20, 26]. The adiponectin
level is decreased in obese subjects, particularly in those
viscerally obese [27]. Reduced adiponectin levels have
also been found to be associated with metabolic syndrome, atherosclerosis, and insulin resistance [20]. Another adipocyte-specific cytokine, leptin, appears to be
influenced by pro-inflammatory cytokines. It has been
suggested that omental fat has more influence than subcutaneous fat on plasma leptin [28]. Similarly, TNF-␣
36
Dermatology 2010;220:32–37
and IL-6 are secreted in adipose tissue and have important roles in the pathogenesis of psoriasis. TNF-␣ and
IL-6 promote a chronic inflammatory state, angiogenesis, and oxidative stress, which contribute to the aetiology
of insulin resistance, glucose intolerance, dyslipidaemia,
hypertension, endothelial dysfunction, and atherogenesis [20, 29].
Viscerally obese patients are more susceptible to
thrombosis and are more likely to show evidence of a
chronic inflammatory state [8]. Obesity has also been
suggested as a risk factor for the development of psoriasis
in a large cohort study [30]. In our study, mean BMI did
not differ significantly between the groups. However, our
study found that the patients with psoriasis had more visceral fat than controls, even when BMI and waist circumference were similar between the two groups. Furthermore, the linear regression model showed that the presence of psoriasis was independently associated with VFA,
suggesting that visceral fat is linked to the chronic inflammatory state. We failed to detect any association between VFA and PASI score or disease duration. The fact
that PASI is not a stable parameter and may change over
time, mainly due to therapy, may explain our failure to
detect a significant association between VFA and PASI
score.
The therapies, particularly systemic steroids, used in
psoriasis may affect the metabolic state of patients. However, no significant association was found between VFA
and the therapies. None of the patients with psoriasis
were receiving systemic steroids. In addition, the study
Balci /Balci /Yonden /Korkmaz /Yenin /
Celik /Okumus /Egilmez
included few patients receiving systemic therapies such
as cyclosporine, methotrexate, or biologics.
In conclusion, for the first time, we demonstrated that
VFA is increased in psoriasis patients and is independently associated with the presence of psoriasis. We also
demonstrated that VFA is independently associated with
the presence of metabolic syndrome in patients with pso-
riasis. Therefore, the increased accumulation of VAT,
which releases pro-inflammatory cytokines, is a potential mechanism linking psoriasis and its metabolic comorbidities and may be a major contributor to the unfavourable cardiovascular risk in psoriasis. Visceral obesity
may be an important target for future interventions in
metabolic comorbidities of psoriasis.
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