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Abstract

Objectives

To assess clinical and laboratory parameters associated with metabolic syndrome in Turkish patients with moderate or severe plaque-type psoriasis and nonpsoriatic controls.

Methods

Patients with moderate or severe plaque psoriasis (patient group) or with nonpsoriatic dermatological disease (controls) were included. Waist circumference, weight, height and arterial blood pressure were measured, together with fasting blood glucose, triglyceride, high density lipoprotein (HDL), fibrinogen, homocysteine and adiponectin levels. Metabolic syndrome was diagnosed using National Cholesterol Education Program–Adult Treatment Panel III criteria.

Results

Out of 90 patients (50 with psoriasis; 40 controls), metabolic syndrome was more frequent in the patient group than in controls. In terms of metabolic syndrome parameters, only hypertension was more frequent in patients with psoriasis compared with controls. There was no statistically significant difference between the patient and control groups for obesity, hypertriglyceridaemia, HDL levels or hyperglycaemia. Fibrinogen levels were increased and adiponectin levels were decreased in the psoriasis group. No between-group difference in homocysteine levels was found.

Conclusion

In this small study, metabolic syndrome was found to be more frequently identified in Turkish patients with psoriasis than in controls; metabolic syndrome could lead to increased cardiovascular disease risk in patients with moderate to severe psoriasis.

Keywords

Psoriasis metabolic syndrome fibrinogen adiponectin

Introduction

Psoriasis is a chronic inflammatory disease affecting ∼0.4–4.7% of the global population,¹ with an aetiopathogenesis that involves attacks mediated by T-helper 1 immune cells. The immune system is known to play a major role in the development and pathogenesis of psoriasis; however, despite numerous studies focused on this disease, the detailed aetiology remains unknown. It is possible that many conditions involving immune and metabolic disorders underlie psoriasis.

The incidence of cardiovascular disease is increased in patients with psoriasis² and the risk of developing cardiovascular disease is predominant in young people with psoriasis.³ Metabolic syndrome (defined according to the unified criteria of the International Diabetes Federation, American Heart Association, National Heart, Lung and Blood Institute)⁴ is characterized by components such as dyslipidaemia, obesity, hypertension and insulin resistance. Metabolic syndrome is a good predictor of cardiovascular disease,⁴ and the increasing prevalence of metabolic syndrome constitutes a major health problem in terms of coronary heart disease, due to the components involved.

The objectives of the present study were to assess clinical and laboratory parameters associated with metabolic syndrome, comparing levels between Turkish patients with moderate or severe plaque-type psoriasis; in addition, levels of these parameters between patients with psoriasis and those with nonpsoriatic dermatological disease were also studied.

Patients and methods

Study population

This cross-sectional study included Caucasian Turkish patients with moderate or severe plaque-type psoriasis and patients with nonpsoriatic dermatological conditions (controls), who presented at the Dermatology Clinic of Gaziantep University, Gaziantep, Turkey between January 2010 and November 2010. Patients ≥18 years of age were sequentially enrolled. Specific inclusion criteria for the patient group were patients with psoriasis who had a psoriasis area and severity index (PASI) score ≥10, and who had not received any systemic treatment (including acidretin, cyclosporine, methotrexate, phototherapy or biological agents) within the previous 3 months.⁵ Specific inclusion criteria for the control group were patients diagnosed with verruca vulgaris, tinea pedis, acne vulgaris, contact dermatitis, lichen planus, neurodermatitis or atopic dermatitis. All study participants provided written informed consent and the study was approved by the local clinical and drug investment ethics committee of Gaziantep University Faculty of Medicine (approval No. 09-2008/170).

Study protocol

Psoriasis area and severity index scores were determined by dividing the body into four sections: head, H (10% of a person's skin); arms, A (20%); trunk, T (30%); legs, L (40%). For each section, the percentage area of skin involved is estimated then transformed into a grade between 0 and 6: grade 0, 0% of involved area; grade 1, <10% of involved area; grade 2, 10–29% of involved area; grade 3, 30–49% of involved area; grade 4, 50–69% of involved area; grade 5, 70–89% of involved area; grade 6, 90–100% of involved area. Within each area, psoriasis severity was estimated by three clinical signs: erythema (redness), induration (thickness) and desquamation (scaling). Severity parameters were measured on a scale of 0–4, where 0 denoted no psoriasis and 4 denoted maximum severity. The sum of all three severity parameters was then calculated for each section of skin, multiplied by the area score for that area and then multiplied by the weight of the respective section (0.1 for H, 0.2 for A, 0.3 for T and 0.4 for L). Each area was scored individually, then the four scores were combined to determine the final PASI score.

Blood pressure, waist circumference, body weight and height were measured for each patient. Serum samples were obtained for assessment of fasting blood glucose, triglycerides, high density lipoprotein (HDL), fibrinogen, homocysteine and adiponectin levels. Blood pressure measurements were performed using an ERKAmeter® 3000 mercury sphygmomanometer (ERKA, Bad Tölz, Germany) with the patient in a seated position, following ≥20 min of rest and no smoking or intake of caffeine for 24 h prior to the measurement. At 08.00 h, following an overnight fast, 10-ml venous blood samples were collected from each study participant into vacutainers without additives. To obtain serum, blood samples were immediately processed by allowing blood to clot at room temperature for 30 min followed by centrifugation at 3000 g for 5 min at 25℃. Serum samples were analysed immediately or stored at 4–6℃ prior to analysis. Serum levels of homocysteine were assessed using a high performance liquid chromatography-based commercial kit (45000 Homocysteine, Reagent kit for HPLC analysis; Chromsystems Instruments and Chemicals GmbH, Munich, Germany) according to the manufacturer’s instructions. Fibrinogen levels were measured by the Clauss clotting method⁶ with Fibri-prest® test kits (Diagnostica Stago, Asnieres sur Seine, France) using a Stago STA Compact Coagulation Analyzer (Diagnostica Stago). Fasting blood glucose, triglyceride and HDL levels were measured with commercial test kits (Roche Diagnostics, Mannheim, Germany) according to the manufacturer’s instructions, using an autoanalyser (Roche/Hitachi Modular DP Systems, Mannheim, Germany). Adiponectin levels were assessed using enzyme-linked immunosorbent assay commercial kits (Zen-Bio, Research Triangle Park, NC, USA) according to the manufacturer’s instructions.

Patients were required to wear light clothes for waist circumference measurements, during which the abdomen was measured at the superior border of the iliac crest. The measurement was performed following normal exhalation with the patient free of any compression. Body mass index (BMI) was calculated by dividing body weight in kg by height in m. Metabolic syndrome was diagnosed according to the National Cholesterol Education Program–Adult Treatment Panel (NCEP–ATP) III criteria⁷ (Table 1).

Table 1.

National Cholesterol Education Program–Adult Treatment Panel (NCEP–ATP) III diagnostic criteria for metabolic syndrome.

Factor	Criteria
Abdominal obesity	Waist circumference >88 cm for women, >102 cm for men
Hypertriglyceridaemia	Fasting triglyceride level ≥150 mg/dl
Low HDL cholesterol	HDL cholesterol <50 mg/dl for women, <40 mg/dl for men
Hyperglycaemia	Fasting blood glucose ≥110 mg/dl
Hypertension	Blood pressure ≥135/85 mm/Hg

HDL, high-density lipoprotein.

Statistical analyses

Statistical analyses of parameters were performed using the SPSS® software package, version 13.0 (SPSS Inc., Chicago, IL, USA) for Windows®. Data were evaluated using descriptive statistics (mean, SD, SE) in addition to independent t-test for paired-group comparisons, χ²-test and Fisher’s exact test for comparison of qualitative data. Results were considered statistically significant at P < 0.05.

Results

A total of 90 patients were enrolled: 50 with moderate or severe plaque-type psoriasis (patient group) and 40 with nonpsoriatic dermatological conditions (control group). The patient group comprised 26 male (52%) and 24 female (48%) patients; the control group comprised 20 male (50%) and 20 female (50%) patients. In the control group, 15 patients were diagnosed with verruca vulgaris, seven with tinea pedis, five with acne vulgaris, five with contact dermatitis, three with lichen planus, three with neurodermatitis and two with atopic dermatitis.

Sex and age distribution patterns were similar between the two groups. Statistical analyses of systolic blood pressure, triglycerides, HDL, fasting blood glucose, waist circumference, BMI, homocysteine, adiponectin and fibrinogen parameters between both groups showed that systolic blood pressure (P = 0.01) and fibrinogen (P < 0.001) levels were higher, and adiponectin levels were lower (P < 0.001), in the patient group than in the control group. There were no between-group statistically significant differences in the other parameters measured (Table 2).

Table 2.

Comparison of age, psoriasis area severity index (PASI) score, systolic and diastolic blood pressure (BP), triglyceride, high-density lipoprotein (HDL), fasting blood glucose, waist circumference, body mass index (BMI), adiponectin, homocysteine and fibrinogen levels between patients with psoriasis and controls (who had nonpsoriatic dermatological conditions).

Characteristic	Patient group n = 50	Control group n = 40	t	Statistical significance
Age, years	38.6 ± 13.2	40.5 ± 14.6	−0.62	NS
PASI score	20.32 ± 5.90	–	–	–
Systolic BP, mmHg	130 ± 17.0	120 ± 15.0	2.60	P = 0.01
Diastolic BP, mmHg	83 ± 14.0	77 ± 11.0	1.96	NS
Triglyceride, mg/dl	177.43 ± 173.91	146.17 ± 84.93	1.05	NS
HDL, mg/dl	41.69 ± 10.50	43.88 ± 10.76	−0.97	NS
Fasting blood glucose, mg/dl	110.92 ± 57.58	95.66 ± 37.63	1.50	NS
Waist circumference, cm	97.20 ± 10.48	94.44 ± 11.07	1.21	NS
BMI, kg/m²	26.92 ± 4.11	25.73 ± 5.89	1.12	NS
Adiponectin, ng/ml	2645.96 ± 1832.92	7641.02 ± 2288.47	−4.59	P < 0.001
Homocysteine, µmol/l	13.64 ± 7.97	13.80 ± 9.77	−0.08	NS
Fibrinogen, mg/dl	358.63 ± 80.91	311.85 ± 72.11	2.86	P < 0.001

Data presented as mean ± SD.

NS, no statistically significant between-group differences (P ≥ 0.05, independent t-test).

Between-group comparisons revealed a significantly higher prevalence of metabolic syndrome in the patient group compared with the control group (25 patients [50%] with psoriasis versus 10 control group patients [25%]; P = 0.01, χ²= 5.84; Figure 1).

Figure 1.

Prevalence of metablic syndrome in patients with psoriasis (n = 50) and controls (n = 40) with nonpsoriatic dermatological conditions. In a total of 25 psoriasis patients and 10 control-group patients (25%) had metabolic syndrome (50%) (P = 0.01, χ²= 5.84, patient group versus control group; χ²-test).

No statistically significant difference was found in the prevalence of metabolic syndrome between male and female patients within the patient and control groups.

Subgroup analyses of age, systolic and diastolic blood pressure, triglycerides, HDL, fasting blood glucose, waist circumference, homocysteine, adiponectin and fibrinogen parameters according to sex (between the patient and control groups) showed that fibrinogen levels were higher (P < 0.001), and adiponectin levels were lower (P < 0.001) in the male patient group compared with the male control group. There were no statistically significant differences in other parameters. Adiponectin levels were significantly lower in the female patient group compared with the female control group (P < 0.001). In addition, there were no statistically significant differences in other parameters between the two female groups.

Subgroup analyses between patients with moderate psoriasis and those with severe psoriasis revealed no statistically significant differences in abdominal obesity, hypertriglyceridaemia, HDL, hyperglycaemia or hypertension levels (Table 3).

Table 3.

Analysis of metablic syndrome parameters between patients with moderate and severe psoriasis, diagnosed according to the National Cholesterol Education Program–Adult Treatment Panel (NCEP–ATP) III criteria.⁷

NCEP–ATP III criteria	Severe psoriasis group n = 35 (70%)	Moderate psoriasis group n = 15 (30%)	Odds ratio (95% CI)
Abdominal obesity, with/without	12/23	4/11	1.43 (0.37, 5.48)
Hypertriglyceridaemia, with/without	6/29	2/13	1.35 (0.4, 7.57)
Low HDL, with/without	10/25	5/10	0.80 (0.21, 2.94)
Hyperglycaemia, with/without	8/27	4/11	0.82 (0.20, 3.30)
Hypertension, with/without	8/27	3/12	1.18 (0.27, 5.20)

Data presented as n patients.

CI, confidence interval.

No statistically significant between-group differences (P ≥ 0.05, χ²-test).

Discussion

Patients diagnosed with psoriasis constitute 0.7–1.3% of polyclinic visits in dermatology departments.^8,9 Psoriasis may be associated with many underlying conditions involving immune and metabolic disorders. Population-based studies have shown a higher risk for mortality in younger patients with severe psoriasis,¹⁰ mainly due to an increased risk of heart attack associated with arterial and venous thrombosis.¹¹ The present study aimed to compare patients with moderate or severe plaque-type psoriasis, to determine the frequency of metabolic syndrome parameters, which are known to be good predictors of cardiovascular disorders. The study involved a small number of patients, which led to a large variance in the data obtained. Indeed, although the odds ratios (OR) showed positive associations (e.g. abdominal obesity [OR 1.43] hypertriglyceridaemia [OR 1.35] and hypertension [OR 1.18]), such differences were not statistically significant: this may have been due to the small sample size, which resulted in wide variations in confidence intervals.

The prevalence of metabolic syndrome was 33.9% in a Turkish population-based study and differed significantly between male (28%) and female (39.6%) participants.¹² The present study revealed no significant difference in the presence of metabolic syndrome between patients of different sexes. However, the prevalence of metabolic syndrome was higher in the psoriasis group and lower in the nonpsoriasis group, compared with overall prevalence of metabolic syndrome reported in the Turkish study.¹² The authors acknowledge that the choice of control group may have affected (and could have biased) the present results. The chosen control group consisted of other patients receiving dermatology care, many of whom were also likely to have low-grade, chronic inflammation that could have led to metoabolic syndrome. This means that the present findings may underestimate the results, because people with other dermatological conditions may not be representative of the general population. For example, acne is known to be associated with a heightened prevalencee of metabolic syndrome.¹³

To the authors’ knowledge, there are no population-based data relating metabolic syndrome and psoriasis in the Turkish population. The existence and magnitude of an association between metabolic syndrome and psoriasis in the general Turkish population, therefore, remains unknown.

In a US population-based study that also used NCEP–ATP III criteria, the prevalence of metabolic syndrome in patients with psoriasis was 40%, which was similar to the prevalence found in the present study.¹⁴ In addition, the prevalence of metabolic syndrome in individuals without psoriasis was approximately half of that found in the patient group.¹⁴

A study in Germany, which compared 541 patients with moderate and severe plaque-type psoriasis with a control group of 1 044 subjects,¹⁵ the prevalence of metabolic syndrome was 25% in patients with psoriasis and 11% in the controls. Prevalence rates for hyperlipidaemia, arterial hypertension, coronary artery disease and type 2 diabetes were higher in patients with psoriasis compared with the control group. Obesity was significantly higher in male compared with female patients.¹⁵ As with the present study, no difference was found between male and female patients with psoriasis, in terms of body weight and incidence of diabetes and coronary artery disease. Another study¹⁶ compared patients with moderate (n = 127 706) and severe (n = 3 854) plaque-type psoriasis with a control group, and included parameters such as hypertension, diabetes, hyperlipidaemia, obesity and smoking (all of which are risk factors for coronary artery disease). In patients with moderate psoriasis, levels of diabetes, hypertension, hyperlipidaemia, obesity and smoking were higher compared with levels observed in the control group. In patients with severe psoriasis, levels of diabetes, obesity and smoking were higher than those observed in the control group. Furthermore, diabetes and obesity were more frequently found in patients with severe compared with moderate psoriasis. The severity of psoriasis may be associated with obesity,^17,18 although it remains unclear whether obesity is a cause or an outcome of psoriasis. In the present study, the authors did not routinely collect information on other possible confounding factors, such as smoking status.

Unlike other published studies, the present study found no difference in BMI and waist circumference measurements between the psoriasis and control groups. In accordance with other studies,^3,11,12 comparison of metabolic syndrome parameters between the moderate and severe psoriasis groups revealed no differences. However, this may be due to the relatively small number of patients in each group, in the present study.

In addition, there was no difference in HDL and triglyceride levels in patients with psoriasis compared with controls, in the present study. Absence of factors such as obesity and diabetes, which have an impact on hyperlipidaemia, may account for the lack of difference in hyperlipidaemia rates between the groups. In a population-based comparative study in the UK, no significant relationship was found between psoriasis and hyperlipidaemia when factors affecting lipid levels (such as obesity and diabetes) were improved in>130 000 patients with psoriasis.¹⁹

Hypertension is reported to be higher in patients with psoriasis compared with controls.^16–20 Echocardiograph and left ventricular abnormalities were also found to be more frequent in patients with psoriasis.²⁰ Similarly, the present study found systolic and diastolic blood pressure to be higher in the psoriasis group compared with in controls. It is likely that hypertension and psoriasis may share common risk factors. For example, angiotensin II – a product of angiotensin converting enzyme (ACE) – is known to regulate vascular tone and stimulate the release of proinflammatory cytokines. Increased levels of serum ACE, in addition to increased serum renin activity, have been reported in patients with psoriasis.^21,22

In the present study, no differences in obesity or hyperglycaemia rates were found between the psoriasis and control groups. However, serum adiponectin levels were lower in patients with psoriasis compared with controls. Adiponectin is a protein-based hormone, produced naturally by the body, that reduces blood vessel tissue inflammation;²³ adiponectin levels are abnormally low in obese patients.²⁴ Lower serum levels of adiponectin without any difference in obesity may suggest that the increased prevalence of cardiovascular disease in patients with psoriasis is related to inflammation in the blood vessels. In the present study, the reduced adiponectin levels observed in patients in the psoriasis group, compared with controls, were inversely correlated with the prevalence of metabolic syndrome, which was higher in the psoriasis group, with no difference between male and female patients. Metabolic syndrome is known to be more prevalent in male patients, although the results of the present study contradict this understanding. This may be due to an unknown mechanism – leading to the development of metabolic syndrome in patients with psoriasis – that affects both sexes.

Increased levels of plasma fibrinogen and homocysteine are risk factors for coronary artery disease.²⁵ An association between increased plasma levels of fibrinogen and metabolic syndrome-related factors such as hyperglycaemia, hypertension and hypertriglyceridaemia has been shown in numerous studies.^26–28 The present study found elevated serum fibrinogen levels in patients with psoriasis, but no difference in homocysteine levels. Due to the limited number of studies, further investigations into the association between psoriasis and prothrombotic and proinflammatory cytokines (such as fibrinogen, homocysteine and adiponectin) are required.

For investigating the possible connections between psoriasis, cardiovascular disease and associated risk factors, Miller et al.²⁹ conducted a meta-analysis of observational studies using random-effects statistics. Of 835 references obbtained in the original search, Miller’s group identified 75 relevant articles that included 503 686 cases and 29 686 694 controls. They found that psoriasis was associated with ischaemic heart disease and cardiovascular risk factors, with the strongest associations being seen in hospital-based studies. Population-based studies did not show significant associations, except for dyslipidaemia.²⁹

In conclusion, the higher prevalence of metabolic syndrome observed in patients with psoriasis in the present study indicates that psoriasis may lead to an increased risk of cardiovascular disease. The finding of reduced adiponectin levels without the presence of obesity may be important, in relation to the tendency of patients with psoriasis to develop cardiovascular disease. The authors believe that improvement of modifiable metabolic syndrome parameters in patients with psoriasis may contribute to a reduction in the risk of cardiovascular disease. Thus, the authors suggest that patients with psoriasis should be evaluated for systemic parameters in addition to skin lesions, and consultations with specialists other than dermatologists should be sought when appropriate.

Footnotes

Declaration of conflicting interest

The authors declare that there are no conflicts of interest.

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

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Clinical and laboratory parameters associated with metabolic syndrome in Turkish patients with psoriasis

Abstract

Objectives

Methods

Results

Conclusion

Keywords

Introduction

Patients and methods

Study population

Study protocol

Statistical analyses

Results

Discussion

Footnotes

Declaration of conflicting interest

Funding

References