|Year : 2019 | Volume
| Issue : 1 | Page : 33-39
Association of leptin, resistin, and high-molecular-weight adiponectin levels with psoriasis area and severity index scores, obesity, and insulin resistance in psoriasis patients
Emine Müge Acar1, Nilsel İlter2, Şehri Elbeg3
1 Department of Dermatology, Kirsehir Ahi Evran University Training and Research Hospital, Kırşehir, Turkey
2 Department of Dermatology, Gazi University Faculty of Medicine, Ankara, Turkey
3 Department of Biochemistry, Gazi University Faculty of Medicine, Ankara, Turkey
|Date of Submission||13-Feb-2018|
|Date of Acceptance||02-Aug-2018|
|Date of Web Publication||28-Mar-2019|
Emine Müge Acar
Kirsehir Ahi Evran University Training and Research Hospital, 2019 Street, No. 1, Kervansaray District, Kirsehir
Source of Support: None, Conflict of Interest: None
Background: Psoriasis is frequently associated with obesity and cardiovascular diseases. Adipocytokines have been implicated in the pathogenesis of psoriasis and its cardiometabolic comorbidities. Objectives: The aim of this study was to assess the roles of leptin, resistin, and high-molecular-weight (HMW) adiponectin in psoriasis as well as their relationship with Psoriasis Area and Severity Index (PASI), obesity, and insulin resistance. Materials and Methods: Forty-six psoriasis patients and equivalent age-, sex-, and body mass index (BMI)-matched controls were recruited in this study. PASI, waist and hip circumferences, and waist/hip ratio (WHR) were recorded, and total body fat mass (TBFM) values were measured using a bioimpedance body composition analyzer. Fasting serum leptin, resistin, and HMW adiponectin levels were measured, and homeostasis model assessment values for insulin resistance (HOMA-IR) were calculated. Results: After the adjustment for anthropometric variables, leptin levels did not differ significantly between the groups (P = 0.736). The patient group showed significantly elevated resistin and lower HMW adiponectin levels (P = 0.007, P= 0.010, respectively). The correlation of serum leptin, resistin, and HMW adiponectin with PASI was not significant (r = −0.100, P= 0.506; r = −0.053, P= 0.726; r = −0.103, P= 0.494, respectively). HOMA-IR positively correlated with leptin and negatively correlated with HMW adiponectin (r = 0.426, P < 0.001; r = −0.393, P < 0.001, respectively). The correlation of leptin and resistin with BMI was direct while that of HMW adiponectin with BMI was inverse (r = 0.532, P < 0.001; r = 0.240, P= 0.021; r = −0.408, P < 0.001, respectively). No significant differences were detected regarding TBFM, and waist and hip circumferences (P = 0.187, P = 0.090, P= 0.543, respectively). However, WHR was significantly higher in the patient group (P = 0.015). Conclusion: Altered adipocytokine levels in psoriasis patients suggest a possible role of adipocytokines in the relationship between psoriasis and its metabolic comorbidities. Fat distribution is also different from the healthy population with similar TBFM values, and abdominal obesity, which is an independent cardiovascular risk factor, is more prevalent in psoriasis patients.
Keywords: Adiponectin, body mass index, insulin resistance, leptin, molecular weight, psoriasis, resistin
|How to cite this article:|
Acar EM, İlter N, Elbeg &. Association of leptin, resistin, and high-molecular-weight adiponectin levels with psoriasis area and severity index scores, obesity, and insulin resistance in psoriasis patients. Dermatol Sin 2019;37:33-9
|How to cite this URL:|
Acar EM, İlter N, Elbeg &. Association of leptin, resistin, and high-molecular-weight adiponectin levels with psoriasis area and severity index scores, obesity, and insulin resistance in psoriasis patients. Dermatol Sin [serial online] 2019 [cited 2020 Oct 28];37:33-9. Available from: https://www.dermsinica.org/text.asp?2019/37/1/33/255040
| Introduction|| |
Psoriasis is a chronic inflammatory skin disease characterized by epidermal hyperproliferation and Th1 cell-mediated inflammation and affects approximately 1%–3% of the population. Obesity has been closely associated with psoriasis, and more severe forms of psoriasis are encountered in obese patients., The severity of obesity also affects treatment response and weight loss reportedly facilitates more favorable treatment outcomes.
Recent studies have shown that the adipose tissue not only plays a role in energy storage but also in endocrinologic and metabolic functions, inflammation, and immunity by employing adipocytokines such as adiponectin, Pre-B cell colony-enhancing factor, visfatin, leptin, resistin, retinol-binding protein 4, tumor necrosis factor-alpha (TNF-α), interleukin-6 (IL-6), and monocyte chemotactic protein-1 (MCP-1 or CCL-2)., Obesity is characterized by low-grade, chronic inflammation; obese patients predominantly secrete proinflammatory cytokines from the adipose tissue, whereas lean individuals release anti-inflammatory cytokines., Recently, it has been suggested that adipocytokines play a role in the pathogenesis of psoriasis and influence its metabolic comorbidities such as obesity and insulin resistance.
Leptin is a 16 kDa adipokine mainly produced by adipocytes and primarily functions as a regulator of appetite, weight gain, and body fat. Besides its metabolic functions, leptin directly or indirectly plays a role in modulating immune response. Leptin promotes Th1 response and suppresses Th2-dependent inflammation and stimulates the release of TNF-α, IL-6, and interferon gamma (IFN-γ) from mononuclear cells. Increasing evidence suggests that leptin is involved in autoimmune diseases including rheumatoid arthritis, diabetes, and psoriasis.
Resistin is an adipokine that was first discovered in rodents in 2001. It was originally implicated in the pathogenesis of diabetes and diabetes–obesity relationship. Recent studies have shown that resistin is involved in inflammation and immunity. Resistin participates in the regulation of proinflammatory cytokine expression and can induce IL-6, IL-8, and TNF-α expression in vitro. Resistin is considered to be involved in TNF-α-related inflammation in psoriasis.
Adiponectin is abundantly found in circulation and has antidiabetic, anti-inflammatory, and vasculoprotective properties. High-molecular-weight (HMW) adiponectin is an adiponectin subtype with a molecular weight of 400–600 kDa and has a higher predictive value for insulin resistance than that of other adiponectin subtypes. Adiponectin is suspected to act as an anti-inflammatory mediator in psoriasis etiopathogenesis, and decreased levels of HMW adiponectin has been reported in psoriasis patients.,
In our study, we aimed to determine the roles of leptin, resistin, and HMW adiponectin in psoriasis, obesity, and insulin resistance by measuring serum adipocytokine levels, homeostasis model assessment-insulin resistance (HOMA-IR) values, and body mass index (BMI), and total body fat mass (TBFM) values of psoriasis patients and comparing these values with those of the age-, sex-, and BMI-matched healthy population.
| Materials and Methods|| |
Recruitment of patients and controls
Forty-six patients who visited our dermatology department between January 2011 and December 2013 and whose diagnosis were confirmed both clinically and histopathologically were recruited. Inclusion criteria were an age of >18 years, disease duration of >1 year, and absence of systemic treatment for the past 1 month. Pregnancy, diabetes, hypertension, and inflammatory diseases other than psoriasis comprised the exclusion criteria. The study was approved by the Local Ethics Committee, and informed consent was obtained from all patients and participants in the control group.
Measurement of adipocytokines
Blood samples were collected from patients and controls after overnight fasting. Serum was extracted after clotting and centrifugation and preserved at − 80°C. Serum leptin (DRG GmbH, Marburg, Germany), resistin (eBioscience, San Diego, California, USA), and HMW adiponectin (RandD Systems Minneapolis, MN, USA) levels were measured using enzyme-linked immunosorbent assay. HOMA-IR was calculated by the following equation: fasting blood glucose × serum insulin level/405.
Measurement of anthropometric values
BMI, waist and hip circumferences, and waist/hip ratio circumference (WHR) values were recorded. Waist circumference was measured from the mid-point of the lowest rib and the iliac crest. Hip circumference was measured at the largest level of the symphysis pubis and gluteus maximus. The TANITA TBF 300 bioimpedance body composition analyzer was used for determining body weight and TBFM values.
The data were analyzed using SPSS for Windows 11.5 program (SPSS Inc., Chicago, IL, USA). Datasets were tested for normality using Shapiro–Wilk test. Descriptive statistics was demonstrated as mean ± standard deviation and median (minimum-maximum) for continuous and discrete variables; categoric variables were demonstrated as number and percentage. Categorical variables were analyzed by Fisher's exact test. The statistical difference between the groups was analyzed using Student's t-test for mean values and Mann–Whitney U-test for median values. Multiple linear regression analyses were performed to determine whether the effect of psoriasis on leptin, resistin, and adiponectin measurements was statistically significant after adjustment for confounding factors (i.e., body weight, BMI, and WHR). Coefficients of regression, 95% confidence intervals and t-statistic for each independent variable were also calculated. Due to the nonnormal distribution, log transformation was applied to leptin, resistin, and adiponectin levels in the multiple linear regression analysis. The correlations between the variables were determined using Spearman's correlation coefficients and a P < 0.05 was considered to be statistically significant.
| Results|| |
The patient group comprised 46 psoriasis patients (29 males and 17 females) and equivalent age-, sex-, and BMI-matched volunteers with no history of skin disease. The Psoriasis Area and Severity Index (PASI) score was 11.2 (4.7–33.2) [Table 1]. Leptin levels did not differ significantly between patients and controls (P = 0.290), whereas serum resistin levels were significantly higher and HMW adiponectin levels were significantly lower in the patient group (P = 0.002 for both). After adjustments for BMI, body weight, and WHR with linear regression analysis, the results persisted; leptin levels were not significantly different between patients and controls, and the patient group showed elevated resistin and lower HMW adiponectin levels (P = 0.736, P = 0.007, P = 0.010, respectively). No significant difference was found in terms of HOMA-IR between the groups (P = 0.430) [Table 2] and [Figure 1]a and [Figure 1]b.
|Table 2: Comparison of serum leptin, resistin and high-molecular-weight adiponectin levels and homeostasis model assessment insulin resistance with control group|
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|Figure 1: (a and b) Serum resistin and high-molecular-weight adiponectin levels in patients and controls|
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PASI levels showed no significant correlations with serum leptin, resistin, and HMW adiponectin levels (r = −0.100, P = 0.506; r = −0.053, P = 0.726; r = −0.103, P = 0.494, respectively). Serum leptin levels and HMW adiponectin levels positively and negatively correlated with HOMA-IR (r = 0.426, P < 0.001; r = −0.393, P < 0.001), respectively. Serum resistin levels did not correlate with HOMA-IR (r = −0.020, P = 0.85). Serum leptin and resistin levels correlated with BMI (r = 0.532, P < 0.001; r = 0.240, P = 0.021, respectively). Serum HMW adiponectin levels inversely correlated with BMI (r = −0.408, P ≤ 0.001) [Table 3] and [Figure 2].
|Table 3: Correlation coefficients and significance values of serum leptin, resistin and high-molecular-weight adiponectin levels and psoriasis area and severity index, homeostasis model assessment insulin resistance and body mass index|
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|Figure 2: Correlation between leptin, resistin and high-molecular-weight adiponectin with body mass index and homeostasis model assessment insulin resistance. (a-c) Leptin and resistin levels show a positive correlation with body mass index, high-molecular-weight adiponectin levels inversely correlated with body mass index (d and e). Leptin levels show positive correlation with homeostasis model assessment insulin resistance, high-molecular-weight adiponectin levels negatively correlate with homeostasis model assessment insulin resistance|
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The body weight and TBFM values of the patient group did not differ from those of the control group (P = 0.270). Waist and hip circumference values of patient and control groups were not significantly different (P = 0.090). However, WHR values of the patient group (0.93 ± 0.07) were significantly higher than those of the control group (0.89 ± 0.07) (P = 0.015) [Table 4].
|Table 4: Comparison of the anthropometric values of patient group with control group|
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| Discussion|| |
Psoriasis is strongly associated with obesity, diabetes, hypertension, metabolic syndrome, and cardiovascular comorbidities; growing evidence has shown that psoriasis is “more than skin deep.”, Chronic inflammation is associated with obesity, which is characterized by abnormal cytokine production, increased synthesis of acute phase reactants, and activation of inflammatory signaling pathways, and has been suggested to increase the risk of psoriasis development. In this study, we noted that serum resistin levels were higher and HMW adiponectin levels of the patients were lower than those of the healthy controls, whereas leptin levels were not significantly different. No correlation between these adipocytokine levels and psoriasis severity was found.
Leptin reportedly stimulates keratinocyte proliferation, adhesion molecule expression, and angiogenesis as well as is likely involved in obesity–psoriasis relationship by inducing or augmenting inflammation. Previous studies concerning leptin levels in psoriasis patients have produced inconsistent results. Elevated and unchanged leptin levels in psoriasis patients have been reported.,,,, In this study, although serum leptin levels were higher in the patient group, the difference was not statistically significant (P = 0.290) and had no correlation with PASI. Consistent with the findings in our study, Johnston et al. and Ozdemir et al. found that leptin levels did not differ between the patient and control groups and did not correlate with disease severity., Serum leptin levels can be affected by many factors such as diet, exercise, anxiety, and depressive mood.,, It is also possible that effects of such factors on leptin levels together with the limited number of patients included in the study and low-PASI levels led to the nonsignificant difference in the leptin levels between the patient and control groups noted in our study.
Resistin was first defined as an adipocyte-secreted peptide that was proposed to be related to obesity and diabetes. Recently,in vivo and in vitro studies have revealed that resistin plays a role in the process of inflammation. Resistin has been shown to stimulate the secretion of TNF-α and IL-12 from macrophages, and TNF-α and IL-1 β, IL-6, or lipopolysaccharides strongly induce resistin expression., Previous studies have reported elevated levels of resistin in psoriasis patients.,,, Consistently, serum resistin levels were significantly higher in the patient group in our study. In the studies conducted by Takahashi et al. and Rajappa et al., a correlation between serum resistin levels and psoriasis severity was reported., As this correlation was not found in our study, we believe that resistin plays a role in psoriasis etiopathogenesis, but serum resistin levels are not associated with disease severity. However, since our study population included a limited number of patients, further studies with larger series investigating the relationship between serum resistin and psoriasis severity are necessary.
Adiponectin circulates in plasma in the form of oligomeric complexes including trimeric, hexameric, and HMW structures. Biological functions of adiponectin have been suggested to be related to its molecular weight., HMW adiponectin is the most active form of adiponectin, and it has been shown to be a more sensitive marker for inflammation and metabolism. Adiponectin has anti-inflammatory functions and inhibits T-cell activation and proliferation as well as decreases TNF-α, IL-6, IFN-γ, and phagocytic activity of macrophages. It has been suggested that adiponectin acts as a protective anti-inflammatory factor in psoriasis. In a study by Nakajima et al., no significant difference was observed between total adiponectin levels of patients and controls, whereas low levels of HMW adiponectin have been reported in psoriasis patients. Shibata et al. also reported decreased levels of HMW adiponectin in psoriasis patients. Consistent with the results of the studies conducted by Shibata et al., and Nakajima et al., we found that HMW adiponectin levels were significantly lower in the patient group. TNF-α and IL-6 inhibit adiponectin synthesis, and thus, elevated IL-6 and TNF-α levels may be responsible for the decrease in adiponectin levels in psoriasis. Nakajima et al. reported that HMW adiponectin levels inversely correlated with psoriasis severity (P = 0.002). In our study, we did not detect a correlation between HMW adiponectin levels and disease severity (P = 0.14). Our results indicate that HMW adiponectin may play a role in psoriasis pathogenesis. The absence of a correlation between HMW adiponectin levels and psoriasis severity may be related to the small size of the patient group and low PASI scores. Therefore, larger studies are required to confirm this relationship.
Consistent with previous studies, leptin and resistin levels directly correlated with BMI values (P < 0,001; P = 0.021, respectively).,, Our results show that serum leptin and resistin levels are related to obesity, and an increase in the number of adipocytes causes an increase in leptin and resistin levels; therefore, they can be used as biomarkers for obesity. In line with the study by Eglit et al., HMW adiponectin levels negatively correlated with BMI in our study. It has been hypothesized that increased synthesis of MCP by hypertrophic adipocytes leads to elevated TNF-α and increased free fatty acid concentrations and results in the suppression of adiponectin secretion. It has been suggested that HMW adiponectin levels are more useful in the prediction of insulin resistance and metabolic syndrome than total adiponectin levels. Our results also confirm that HMW adiponectin is a sensitive biomarker for the assessment of metabolic risk.
Leptin has been implicated in glucose homeostasis and insulin sensitivity regulation. A significant correlation between HOMA-IR and serum leptin levels has been reported in previous studies., Our study also demonstrated that serum leptin levels directly correlated with HOMA-IR values, indicating a relationship between leptin and insulin resistance. On the contrary, the role of resistin in insulin resistance remains controversial.,, Our results show that serum resistin is not directly involved in insulin resistance because no correlation between serum resistin levels and HOMA-IR values was detected. In line with the study by Eglit et al., our results suggested that HMW adiponectin levels inversely correlated with HOMA-IR value. Adiponectin is a beneficial cytokine owing to its anti-inflammatory, antiatherogenic, antidiabetic, and cardioprotective effects. Our results support the hypothesis that low levels of adiponectin are associated with increased metabolic risk and that HMW adiponectin may play a protective role against insulin resistance.
In this study, no statistically significant difference in TBFM values between the groups was detected. Mashayekhi-Goyonlo et al. reported that total fat mass percentages did not differ between the groups, whereas abdominal fat mass percentages were significantly higher in the patient group. Central obesity, characterized by an increase in abdominal fat mass values, is a marker representing high risks of insulin resistance and metabolic syndrome development. Because we did not measure abdominal fat mass values, we believe that the sole measurement of TBFM may be insufficient for estimating metabolic risk. However, WHR, which is also a marker for abdominal obesity was found to be significantly higher in the patient group than that in the control group. Waist circumference and WHR have been reported to be independently associated with type 2 diabetes mellitus, arterial disease, and mortality risk., WHR has been suggested to be a more reliable risk factor for myocardial infarction (MI) comparing to waist circumference. Psoriasis has been demonstrated to be associated with cardiovascular morbidities and independently associated with increased MI risk. Our results reveal that psoriasis patients have increased the risk of cardiovascular morbidities.
| Conclusion|| |
Our results indicate that resistin and HMW adiponectin levels are altered in comparison with the BMI-matched healthy population that has similar TBFM values. Leptin and HMW adiponectin are associated with insulin resistance. Leptin, resistin, and HMW adiponectin levels facilitate the assessment of obesity-related inflammation. This study supports the view that adipocytokines may play a role in the relationship between psoriasis and its metabolic comorbidities. Our study also indicates that fat distribution in psoriasis patients is different from the healthy population with similar TBFM values and that abdominal obesity, which is an independent cardiovascular risk factor, is more prevalent in psoriasis patients. Further large-scale studies are necessary to examine and determine the role of adipocytokines in psoriasis pathogenesis and its comorbidities.
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Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3], [Table 4]