Mariame Meziane1, MD, Awatef Kelati1, MD, Adil Najdi2, MD, Amine Berraho2, MD,
Chakib Nejjari2, MD, and Fatim-Zahra Mernissi1, MD
Department of Dermatology, University Hospital Hassan II, and 2Laboratory of Statistics and Clinical Research, Faculty of Medicine and Pharmacy, Fes, Morocco
Background Several recent reports have shown a significant association between psoriasis and metabolic syndrome (MBS).
Objective The goal of this study was to investigate the prevalence of MBS and, in particular, the main factors that determine this syndrome in Moroccan patients with psoriasis.
Methods A case–control study has included 150 patients with psoriasis and 300 controls matched for age and sex, the MBS was defined according to the International Diabetes Foundation, and the severity of psoriasis was assessed by body surface area.
Results Mild psoriasis was seen in 10.7%, 40.3% had moderate psoriasis, and 49% had severe psoriasis. MBS was higher in cases than in controls with statistical differences (44.7 vs. 2.7%, odds ratio [OR]: 26 CI: [12.4–54.3]; P = 0.000). Abdominal obesity and dyslipidemia were the only metabolic factors significantly related to psoriasis whereas diabetes, hypertension, smoking, alcohol consumption, and cardiovascular diseases were not significant. MBS increases with age in our patients with psoriasis, whereas there was no relationship between MBS and gender. Hypertension (P = 0.007), diabetes (P = 0.003), and increased level of triglycerides (P = 0.05) and high-density lipoprotein cholesterol
(P = 0.003) were associated with the severity of psoriasis.
Conclusion Metabolic syndrome is an important comorbidity in patients with psoriasis, and vigilance and enhanced screening may be important in this population, especially patients with severe disease.
Psoriasis is a chronic inflammatory skin disease characterized by erythematous, scaly patches on different areas of the body. A multifactorial disease affects 2–3% of the general population.1 It is currently believed that the skin component in psoriasis is visible but extracutaneous events are underestimated and that psoriasis is linked to a number of behavioral and systemic comorbidities in many patients.
The metabolic syndrome (MBS) is a group of clinical and biological disorders that include abdominal obesity, glucose intolerance, hypertension, and dyslipidemia.2 Many organizations have proposed criteria for the diagnosis of MBS, including the World Health Organization,3 the National Cholesterol Education Program Adult Treatment Panel III (NCEP ATP III),4 and the International Diabetes Foundation.5 Recent reports have shown a significant association between psoriasis and MBS; the main mechanism implicated in both pathologies seems to be inflammation.6 Most of those studies have been done in occidental countries,7–10 some of them in North Africa,11 but none have been reported in Morocco.
The aim of this study is to determine the prevalence of MBS and, in particular, the main factors that determine this syndrome in Moroccan patients with psoriasis.
Materials and methods
This was a hospital-based case–control study and the protocol was proposed by the Department of Epidemiology and Clinical Research in Fes.
It was a matched case–control and unicentric study with a prospective data collection of patients with psoriasis followed at the Department of Dermatology, University Hospital Hassan II (Fez, Morocco), which were either inpatients or outpatients during the period from November 2011 to November 2012.
Cases were consecutive subjects with psoriasis (confirmed clinically and/or histologically), aged more than 15 years old.
Exclusion criteria were pregnancy and those who received systemic treatment for psoriasis, including acitretin and cyclosporine for at least 1 month before enrollment.
Controls were patients followed for dermatological diseases other than psoriasis who presented during the same period. For each case, we had identified two non-psoriatic controls of the same sex and age ( 3 years).
All patients were classified into two age groups: between 15 and 45 years and above 45 years.
For subjects and controls, a detailed history taking included duration of the disease, joint pains, smoking, alcohol consumption, diet, presence of other systemic illness, past intake of systemic agents for psoriasis, and concomitant intake of medicines for other illnesses was collected. Clinical examination included measurement of height, weight, waist circumference, and blood pressure. Biological exams included measurement of glycemia, cholesterol, and triglycerides (TGs).
The severity of psoriasis was estimated by calculating the body surface area (BSA) according to the survey by Langan et al ;12 mild psoriasis was defined as ≤2% of the BSA, moderate psoriasis as between 3 and 10% of the BSA, and severe psoriasis >10% of the BSA.
Metabolic syndrome was defined according to the International Diabetes Foundation.5 According to this
foundation, and based on Mediterranean ethnicity, MBS is diagnosed when a person has at least three of these five conditions: fasting glucose 100 mg/dl or greater (or receiving drug therapy for hyperglycemia), blood pressure 130/85 mmHg or higher (or receiving drug therapy for hypertension), TGs 150 mg/dl or higher (or receiving drug therapy for hypertriglyceridemia), high-density lipoprotein cholesterol (HDLC)
level <40 mg/dl in men or <50 mg/dl in women (or receiving drug therapy for reduced HDL-C), and waist circumference 94 cm or greater in men or 80 cm or greater in women.
The waist circumference was measured by placing the measuring tape snugly around the abdomen at the level of the iliac crest.
The blood pressure was taken in the sitting position, and the average of two measurements was recorded. Hypertension was defined according to the definition of MBS described previously.
Venous blood samples were collected from fasting subjects; glycemia was measured using a glucose oxidase method.
Cholesterol and TGs were measured using enzymatic methods. HDL-C was measured using a direct method.
Data were analyzed using the Statistical Package for the Social Studies version 20 (SPSS 20; SPSS Inc., Chicago, IL, USA).
Metabolic syndrome and its components were first compared between cases and controls, we then compared MBS with demographic and clinical factors, and then we investigated the relation between psoriasis severity and MBS factors.
Three analyses were performed:
● Descriptive analysis: quantitative variables were expressed as means standard deviation and qualitative variables as percentages.
● Univariate analysis: comparison of two percentages was carried out by the McNemar test, comparison of several percentages by the Freedman test, and comparison of averages was done with Student’s and ANOVA tests.
● Multivariate analysis was performed by the conditional regression method. P < 0.05 was considered statistically significant.
Our study included 150 patients with psoriasis and 300 controls matched for age and sex. The mean age of our patients was 40.8 years 15.5; psoriasis was observed more in young subjects (under 45 years old). There was no sex predominance, and 13.3% of patients with psoriasis had a family background of this condition. MBS was significantly more common in patients with psoriasis than in controls (44.7 vs. 2.7%; odds ratio [OR]: 26 CI: 12.4– 54.3; P = 0.000).
We calculated the prevalence of MBS and its factors in cases and in controls. In the univariate analysis, all variables studied were significant in our study population, including familial cases of psoriasis, abdominal obesity, hypertension, diabetes, a low rate of HDL-C, and a high rate of TG, in addition to some cardiovascular risk factors such as smoking and alcohol consumption. Only cardiovascular
diseases were not significant. In the multivariate analysis, only abdominal obesity and dyslipidemia
remained significant. Abdominal obesity was the factor most associated with psoriasis, so that the increase in the waist of 1 cm increases the risk of MBS of 9. The psoriasis was also associated with a low rate of HDL-C and a high rate of TG and hypertension. All these factors are summarized in Table 1.
The study of demographics and clinical factors that influence MBS showed that MBS increases with the age of our patients with psoriasis, whereas there was no relationship between MBS with gender or with the disease duration and the psoriasis severity in our patients with psoriasis. These results are summarized in Table 2.
Otherwise, the MBS components were associated with the severity of psoriasis in the sense that the presence of MBS increases the severity of the disease, except for abdominal obesity where this link was not significant (Table 3).
This paper reports the results of the first case–control study that has investigated MBS in Moroccan patients with psoriasis. Our study reveals that MBS was higher in cases than in control subjects, that MBS increased with age of our cases, and that MBS components were associated with the severity of psoriasis.
The majority of occidental studies have found a significant association between MBS and psoriasis.5,7–14 In our study, there was also a strong association between psoriasis and MBS in cases (44.7%) versus only 2.7% in controls with (OR); 26 CI, 12.4–54.3; P = 0.000. This can be explained by the type of diseases in control subjects (onychomycosis, lipomas, vitiligo, skin cancer, etc.), the role of genetic predisposition in patients with psoriasis to develop MBS, and the definition used for MBS (the International
Diabetes Federation definition instead of the NCEP-ATPIII definition used in most of the studies).
Another hypothesis could be the Mediterranean diet that we share with other Mediterranean countries such as Spain and Italy (a diet rich in vegetables and olive oil).
However, a Tunisian survey11 of 164 patients with psoriasis and 216 controls found a lack of association between the prevalence of MBS in cases and in controls (35.5 vs. 30.8%).
Metabolic syndrome increases with age in our patients with psoriasis, whereas there was no relationship between MBS and gender, which is different from the Tunisian study, as prevalence of MBS was significantly increased only in psoriatic women (P = 0.01).11 Concerning the duration of psoriasis, there was no significant association between this variable and MBS in our patients with psoriasis, while in a Tunisian study, the prevalence of MBS was higher in patients with psoriasis for more than 10 years than in patients with psoriasis for <10 years (22 vs. 46.4%, P = 0.024).11 In addition, Gisondi et al.15 noted that patients with psoriasis with MBS had a longer disease duration compared with patients with psoriasis without MBS. Our results may be explained by the fact that more than half of our patients
had psoriasis only for <5 years. We also observed that psoriasis was associated with abdominal obesity, a high rate of TG, and low rate of HDL-C. Concerning abdominal obesity and hypertriglyceridemia, their association with psoriasis was documented in Italian (P = 0.01 and P = 0.001, respectively) and Indian (P = 0.035 and P = 0.011, respectively) studies. 9,16 Besides, the low rate of HDL-C was the only significant parameter in the Tunisian study.11 Even diabetes mellitus and hypertension are reported
more frequently among patients with psoriasis; we did not find a significant association between MBS and these two parameters in our patients. This was consistent with the Tunisian study11 but was different from other reports.16,17 We concluded that diabetes mellitus and elevated blood pressure did not have a clinical significance in our patients with psoriasis. Smoking, alcohol consumption, and cardiovascular diseases were not associated with psoriasis in our survey, contrary with the results found in some other studies18–20 and identical to the results of Wakkee et al.21 Several studies have found that MBS is an aggravating factor in the prognosis of psoriasis.22,23 The majority of those series have used the psoriasis area and severity index (PASI) to appreciate the disease severity. In our study, the severity of psoriasis was estimated using the BSA.12 Like Langan et al., we found that the association
between MBS and psoriasis increased with increasing disease severity. In a Japanese survey, patients with psoriasis with MBS showed a significantly higher PASI score than those without MBS (PASI > 10).24 However, in a Tunisian and an Italian series, prevalence of MBS was not influenced by psoriasis severity.11,15 Furthermore, we also found that associations with all variables of MBS were significantly linked with disease severity except for abdominal obesity. In an earlier report, Rosa et al.25 found that parameters of MBS were not related to psoriasis severity. Abdominal obesity, which is the main criteria of MBS definition, was significantly related to psoriasis and not to its severity in our study; we think that this factor must be taken into account in psoriasis management whatever its severity.
Our study had some limitations. First, the use of the BSA instead of PASI to assess psoriasis severity, the definition chosen for MBS, which is based on ethnicity5 rather than another definition, and finally, the inclusion of all cases of psoriasis regardless of their clinical presentation.
The results of this study confirmed that MBS is an important comorbidity in patients with psoriasis and that vigilance and enhanced screening may be important in this population, especially patients with severe disease. All dermatologists should be aware that MBS and its individual components might be associated with psoriasis during the course of the disease.
1 Gudjonsson JE, Elder JT. Psoriasis: epidemiology. Clin Dermatol 2007; 25: 535–546.
2 Eschwege E. Metabolic syndrome: which definition(s) for which objective(s)? Ann Endocrinol 2005; 66: 1S32–1S44.
3 Alberti KG, Zimmet PZ. Definition, diagnosis and classification of diabetes mellitus and its complications.
Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet Med 1998; 15: 539–553.
4 Expert Panel on Detection. Evaluation, and treatment of high blood cholesterol in adults. executive summary of the third report of the national cholesterol education program (NCEP) expert panel on detection, evaluation and treatment of high blood cholesterol in adults (adult treatment panel III). JAMA 2001; 285: 2486–2497.
5 Takahashi H, Iizuka H. Psoriasis and metabolic syndrome. J Dermatol 2012; 39: 212–218.
6 Bens G, Maccari F, Esteve E. Psoriasis: a systemic disease. Press Med 2012; 41: 338–348.
7 Shapiro J, Cohen AD, Weitzman D, et al. Psoriasis and cardiovascular risk factors: a case-control study on inpatients comparing psoriasis to dermatitis. J Am Acad Dermatol 2012; 66: 252–258.
8 Sommer DM, Jenisch S, Suchan M, et al. Increased prevalence of the metabolic syndrome in patients with moderate to severe psoriasis. Arch Dermatol Res 2006; 298: 321–328.
9 Gisondi P, Targher G, Zoppini G, et al. Non-alcoholic fatty liver disease in patients with chronic plaque
psoriasis. J Hepatol 2009; 51: 758–764.
10 Augustin M, Reich K, Glaeske G, et al. Co-morbidity and age-related prevalence of psoriasis: analysis of health insurance data in Germany. Acta Derm Venereol 2010; 90: 147–151.
11 Mebazaa A, El AsmiM, Zidi W, et al. Metabolic syndrome in Tunisian psoriatic patients: prevalence and determinants. J Eur Acad Dermatol Venereol 2011; 25: 705–709.
12 Langan SM, Seminara NM, Shin DB, et al. Prevalence of metabolic syndrome in patients with psoriasis: a population-based study in the United Kingdom. J Invest Dermatol 2012; 132: 556–562.
13 Love TJ, Qureshi AA, Karlson EW, et al. Prevalence of the metabolic syndrome in psoriasis: results from the national health and nutrition examination survey, 2003- 2006. Arch Dermatol 2011; 147: 419–424.
14 Arias-Santiago S, Orgaz-Molina J, Castellote-Caballero L, et al. Atheroma plaque, metabolic syndrome and inflammation in patients with psoriasis. Eur J Dermatol 2012; 22: 337–344.
15 Gisondi P, Tessari G, Conti A, et al. Prevalence of metabolic syndrome in patients with psoriasis: a hospitalbased case-control study. Br J Dermatol 2007; 157: 68–73.
16 Madanagobalane S, Anandan S. Prevalence of metabolic syndrome in South Indian patients with psoriasis vulgaris and the relation between disease severity and metabolic syndrome: a hospital-based case-control study. Indian J Dermatol 2012; 57: 353–357.
17 Zindanci I, Albayrak O, Kavala M, et al. Prevalence of metabolic syndrome in patients with psoriasis. Sci World J 2012; 2012: 312463.
18 Shin DB, Wang X, Margolis DJ, et al. Prevalence of cardiovascular risk factors in patients with psoriasis. J Am Acad Dermatol 2006; 55: 829–835.
19 Mehta NN, Azfar RS, Shin DB, et al. Patients with severe psoriasis are at increased risk of cardiovascular mortality: cohort study using the general practice research database. Eur Heart J 2010; 31: 1000–1006.
20 Brauchli YB, Jick SS, Miret M, et al. Psoriasis and the risk of incident myocardial infarction, stroke or transient ischemic attack: an inception cohort study with a nested case-control analysis. Br J Dermatol 2009; 160: 1048– 1056.
21 Wakkee M, Herings RM, Nijsten T. Psoriasis may not be an independent risk factor for acute ischemic heart disease hospitalizations: results of a large populationbased Dutch cohort. J Invest Dermatol 2010; 130: 962– 967.
22 Naldi L, Chatenoud L, Linder D, et al. Cigarettes smoking, body mass index, and stressful life events as risk factors for psoriasis: results from an Italian casecontrol study. J Invest Dermatol 2005; 125: 61–67.
23 Kimball AB, Guerin A, Tsaneva M, et al. Economic burden of comorbidities in patients with psoriasis is substantial. J Eur Acad Dermatol Venereol 2011; 25: 157–163.
24 Chen YJ, Wu CY, Shen JL, et al. Psoriasis independently associated with hyperleptinemia contributing to metabolic syndrome. Arch Dermatol 2008; 144: 1571– 1575.
25 Rosa DJ, Machado RF, Matias FA, et al. Influence of severity of the cutaneous manifestations and age on the prevalence of several risk factors in patients with psoriasis. J Eur Acad Dermatol 2012; 26: 348–353.