Psoriasis and metabolic syndrome in children: current data

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1 Original article CED Clinical and Experimental Dermatology Psoriasis and metabolic syndrome in children: current data A. Pietrzak, 1 E. Grywalska, 2,3 M. Walankiewicz, 2 T. Lotti, 4 J. Rolinski, 2,3 W. Myslinski, 5 P. Chabros, 1 D. Piekarska-Myslinska 1 and K. Reich 6 1 Department of Dermatology, Venereology and Paediatric Dermatology; 2 Department of Clinical Immunology and Immunotherapy and 5 Department of Internal Diseases, Medical University of Lublin, Lublin, Poland; 3 St. John s Cancer Center, Lublin, Poland; 4 Department of Dermatology, University of Rome G. Marconi, Rome, Italy and 6 Dermatologikum Hamburg and SCIderm Research Institute, Hamburg, Germany doi: /ced Summary Background. The prevalence of cardiovascular and metabolic disorders in paediatric patients with psoriasis is not well established. Aim. To conduct a meta-analysis of previously published studies dealing with the occurrence of metabolic disorders in children with psoriasis. Methods. Data from 7 studies with a total of 965 children with psoriasis were analysed using a random effects model. Results. Prevalence of metabolic syndrome (MetS) was significantly higher in patients with psoriasis than in healthy controls (HCs). In most studies, significantly decreased levels of high-density lipoprotein (HDL) cholesterol were found in children with psoriasis. Mean level of HDL cholesterol in patients with psoriasis was 2.05 mg/dl lower than in HCs. Patients with psoriasis and HCs did not differ significantly in their mean triglyceride levels, although the difference was at a threshold of statistical significance. Mean level of fasting glucose in children with psoriasis was 5.75 mg/dl higher than in HCs (P < 0.01). The two groups did not differ significantly in mean waist circumference or in systolic and diastolic arterial pressures. Conclusions. Decreased levels of HDL cholesterol and increased concentrations of fasting glucose may represent very early stages of MetS in children with psoriasis. However, a large population-based study is needed to establish the relationship between psoriasis and MetS in children, including the environmental, genetic and immunological factors leading to their co-occurrence. Introduction Psoriasis is a multifactorial, immune-mediated skin disease, characterized by a variety of inflammatory disturbances, hyperkeratotic plaques, recurring lesions and involvement of the joints. Psoriasis affects approximately 2 5% of the population. 1 Augustin et al. 2 estimated the overall 1-year prevalence of this condition Correspondence: Dr Aldona Pietrzak, Department of Dermatology, Venereology and Paediatric Dermatology, Medical University of Lublin, 13 Radziwiłłowska Str., Lublin, Poland aldonapietrzak@umlub.pl Conflict of interest: the authors declare that they have no conflicts of interest. Funding: The study was supported from DS 168 grant from the Medical University of Lublin. Accepted for publication 20 March 2016 at 2.53%, and its total prevalence in children up to 18 years of age at 0.71% (0.66% and 0.76% for boys and girls, respectively). The prevalence increased in an approximately linear manner, from 0.12% at 1 year of age to 1.24% at 18 years. 2 A wide range of comorbidities may co-exist with psoriasis, with the most important being cardiovascular disease (CVD) and its risk factors: obesity, arterial hypertension (AHT), dyslipidaemia (DLP) and type 2 diabetes mellitus (T2DM). This implies that psoriasis may be associated with increased risk of metabolic syndrome (MetS), defined as the presence of at least three of five of the following conditions: abdominal obesity, elevated blood pressure, elevated fasting plasma glucose, high levels of serum triglycerides and low levels of high-density lipoprotein (HDL) cholesterol. 3 All these comorbidities commonly occur in Clinical and Experimental Dermatology 1

2 adult psoriasis, 3 but their prevalence in paediatric patients is not well established, because of the small number of studies and participants. Therefore, the aim of this study was to conduct a meta-analysis of previously published studies dealing with the occurrence of metabolic disorders in children with psoriasis. 4 Methods A search of the MEDLINE and EMBASE databases from 1966 to June 2015 was carried out, using the relevant MeSH terms including all sub-headings. This was combined with a keyword search using cardiovascular OR apolipoprotein OR apolipoproteins OR dyslipidemia OR dyslipidaemia OR hypercholesterolemia OR hypertriglyceridemia OR triglyceride OR triglycerides OR lipid OR lipids OR cholesterol OR HDL OR LDL OR lipoprotein OR lipoproteins OR body mass index OR BMI AND psoriasis OR psoriatic AND child OR children OR pediatric OR pediatrics OR infant OR infants OR newborn OR newborns. Two authors (AP and KR) performed the searches independently and reviewed the results according to the Newcastle-Ottawa Scale for assessing the quality of nonrandomized studies in meta-analyses. All discrepancies were resolved by consensus. We searched for English-language publications and human studies. Review articles, abstracts and editorials were excluded, and duplicate data were removed. Data were extracted from the publications independently by the two reviewers, and the following information was recorded: first author, year of publication, country, study design, number of patients, incidence of MetS and its components (fractions of participants meeting the diagnostic criteria for MetS overall and for its individual components) and/or values of determined metabolic parameters (blood concentrations of glucose, triglycerides and HDL cholesterol, systolic and diastolic blood pressure, and waist circumference). In total, 122 articles were found by the electronic searches. After exclusion of conference abstracts (n = 58) and of studies that did not meet the inclusion criteria based on their title and abstract (n = 43), 21 papers remained. After reviewing the full texts, 7 relevant studies 4 10 with a total of 965 children with psoriasis were eligible for inclusion in the study. the results are presented as mean differences (D) or OR with 95% CI. Homogeneity of the studies was verified with T2 test based on the weighted least squares method. The threshold of statistical significance for all the analyses was set at P Results Metabolic syndrome Prevalence of MetS was assessed in 3 studies with a total of 60 children with psoriasis (Fig. 1). In all these studies, prevalence of MetS was significantly higher in patients with psoriasis than in healthy controls (HCs) (OR = 6.10, 95% CI ; P < 0.001). All the studies were homogeneous (P = 0.896). High-density lipoprotein cholesterol In all but one of the seven studies, significantly decreased levels of HDL cholesterol were found in children with psoriasis (P = 0.03). Mean level of HDL cholesterol in children with psoriasis was 2.05 mg/dl lower than in HCs (95% CI 3.89 to 0.21 mg/dl; Fig. 2), and the studies were heterogeneous (P < 0.001). Triglycerides Serum concentrations of triglycerides were measured in 536 children with psoriasis. Patients with psoriasis and HCs did not differ significantly in their mean triglyceride levels, although the difference was at a threshold of statistical significance (D = 8.69 mg/dl, Statistical analysis Results were analysed with Statistica software (v10; StatSoft, Tulsa, OK, USA), using a random effects model. Depending on the type of analysed variables, Figure 1 Forest plot illustrating odds ratios (ORs) for metabolic syndrome in psoriatic vs. non-psoriatic children documented in previous studies. 4,7,9 2 Clinical and Experimental Dermatology

3 Other parameters There was no difference in mean systolic or diastolic arterial pressures or in waist circumference between children with psoriasis and HCs (P = 0.06, P = 0.78, P = 0.20, respectively). Discussion Figure 2 Forest plot illustrating mean differences (D) in serum HDL cholesterol levels in psoriatic and non-psoriatic children examined in previous studies. 4 6,8,9 Figure 3 Forest plot illustrating mean differences (D) in serum fasting glucose levels in psoriatic and non-psoriatic children examined by previous studies. 4,8,9 95% CI 0.26 to mg/dl; P = 0.06). The studies were heterogeneous (P < 0.001). Fasting glucose Mean level of fasting glucose in 40 children with psoriasis was significantly higher than in HCs (P < 0.01), with D = 5.75 mg/dl (95% CI mg/dl; Fig. 3). The analysed studies were heterogeneous (P = 0.03). MetS is a cluster of cardiometabolic risk factors, including central obesity, insulin resistance, glucose intolerance, DLP and increased blood pressure. 11 Aside from CVD and T2DM, MetS is also associated with many other clinical conditions, such as chronic lowgrade inflammation, oxidative stress, hyperuricaemia, dyslipidaemia, hyperandrogenism, polycystic ovary syndrome, hepatic steatosis and non-alcoholic fatty liver disease, impaired glucose tolerance, obstructive sleep apnoea, hypogonadism, vascular dementia, Alzheimer disease and some cancers. 12 The definition of MetS in children and adolescents has raised controversy, as no clear thresholds for metabolic parameters exist for this group. 13,14 Nevertheless, it has been shown that children with MetS are at increased risk of adult MetS as well as, T2DM and CVD. 15 MetS comprises a complex phenotype that correlates with obesity, but nonetheless appears to be distinct. Metabolic diseases, such as obesity and T2DM, have a common genetic background with psoriasis. 16 Moreover, they appear to interact at a functional level, because both obesity and the upregulation of proinflammatory mediators observed in psoriasis seem to influence adipocyte homoeostasis, inducing nonprofessional immune functions, which may perpetuate psoriatic inflammation. In addition, a disturbed adipokine profile and psoriasis-associated inflammation may induce insulin resistance and lead to CVD. 17 There appears to be an important role of tumour necrosis factor-a and other factors that are overproduced in patients with psoriasis, as these may contribute to the elevated risk of MetS. 18 The metabolic profile of children with psoriasis has been examined in a relatively small number of studies. Thus, we decided to perform a meta-analysis of the available data based on the results of seven studies in children with psoriasis. We analysed blood concentrations of HDL cholesterol, triglycerides and fasting glucose, as well as waist circumference and systolic and diastolic blood pressure. Concentrations of HDL cholesterol were available in six studies, and data on waist circumference, blood pressure and fasting glucose in Clinical and Experimental Dermatology 3

4 three. Our meta-analysis showed that children with psoriasis had significantly lower levels of HDL cholesterol and significantly higher concentrations of fasting glucose compared with HCs. The two groups did not differ significantly in systolic and diastolic pressures, triglyceride concentrations or waist circumference. Noticeably, a study conducted by Toruniowa et al. 5 showed significant differences in mean levels of triglycerides in both boys and girls with psoriasis. No sex-specific analyses of metabolic parameters were included in the other studies. Decreased concentrations of HDL cholesterol are typically observed in patients with T2DM. The aetiology of this abnormality still remains unclear. It has been suggested that insulin resistance, enhanced synthesis of very low-density lipoprotein (LDL), and increased activities of cholesteryl ester transfer protein and endothelial lipase may play an important role in lowering HDL cholesterol concentrations. 19 The results of the seven studies included in our meta-analysis strongly support suggestions that psoriasis is an inflammatory disorder that not only affects the skin, but also leads to metabolic disorders. Decreased levels of HDL cholesterol and increased concentrations of fasting glucose may represent the very early stages of a psoriasis-related metabolic disorder. It should be emphasized, however, that the participants in the analysed studies were very young and it is possible that, despite the presence of active psoriasis and some metabolic abnormalities, they would not go on to develop cardiovascular complications such as systemic hypertension or visceral obesity. Our findings imply that the levels of plasma lipids, insulin resistance and glucose (in a fasted state or during oral glucose tolerance test) should be monitored in all paediatric patients with psoriasis to detect any abnormalities early and thereby prevent clinically significant cardiovascular disorders. Augustin et al. 2 found that the overall prevalence of comorbidities in patients with psoriasis aged < 20 years was double that of people without this condition, and juvenile psoriasis was shown to be associated with higher prevalence of DLP, obesity, AHT, DM, rheumatoid arthritis and CVD. Interestingly, CVD occurred 3 4 times more often in patients with psoriasis than in HCs, and the prevalence of DLP, diabetes mellitus and AHT in patients with psoriasis was double that of the general population. Another study conducted by Augustin et al., 20 based on data from a German database, demonstrated that children with psoriasis are at increased risk of DLP, DM, AHT and obesity. Similar results were obtained in Chinese and Italian studies, as reviewed by Wootton and Murphy. 21 A significant association between paediatric MetS and CVD risk was also demonstrated in a longitudinal study with a 25-year follow-up. 22 Previous studies of psoriasis-specific changes in serum concentrations of lipids in children are sparse and have produced inconclusive results. Toruniowa et al. 5 analysed the serum lipid profiles of children aged 6 14 years: 47 children with generalized psoriasis (14 boys, 33 girls) and an HC group (19 boys, 15 girls). Psoriasis was shown to be associated with a decrease in HDL levels in both sexes [patients with psoriasis vs. HCs: mg% vs (P < 0.03) for boys, and vs mg% (P < 0.05) for girls]. There was an interesting observation for triglyceride concentration in boys with psoriasis, in whom this parameter increased to vs in HCs (P < 0.09). No statistically significant differences were found for total or LDL cholesterol. According to Toruniowa et al. 5 an atherogenic pattern of lipid metabolism disorders might already developed in their participants. The reasons behind the decrease in HDL cholesterol level at such a young age remain unclear. Perhaps this phenomenon may be associated with impaired synthesis of HDL cholesterol in the liver or intestines, or with impaired homeostasis at the cellular level. 5 Koebnick et al. 6 conducted a large population-based study and showed an association between the occurrence of psoriasis and weight gain in children. Overweight and obesity were shown to be associated with an increased risk of psoriasis in youth. Irrespective of their body weights, adolescent patients with psoriasis presented with significantly higher concentrations of total cholesterol, LDL cholesterol, triglycerides and alanine aminotransferase. 6 Matusiewicz et al. 23 explored the epidemiology, treatment and comorbidities of patients with juvenile psoriasis in Germany, using health insurance data for 4499 children and adolescents ( 18 years of age). Prevalence of comorbidities was estimated at 0.4%, ranging from 0.1% at 1 year of age to 0.8% at 18 years of age. Consequently, childhood psoriasis seems to be associated with a significantly greater comorbidity rate than that in children without this condition. 23 Augustin et al. 20 showed that a distinct group of comorbidities, previously attributed solely to adult psoriasis, may also develop in children with psoriasis. In their study, children with psoriasis were found to have hyperlipidaemia, T2DM, hypertension, obesity and ischaemic heart disease markedly more often than HCs, implying that the 4 Clinical and Experimental Dermatology

5 signs of MetS may emerge irrespective of patient age and duration of psoriasis. Moreover, the results of that study 20 indicated the possible presence of separate mechanisms leading to clinical disease in psoriasis and MetS. A number of authors have suggested monitoring patients with psoriasis. Au et al. 7 suggested that children with psoriasis should be subject to primary prevention measures for CVD, while Koebnick et al. 6 stated that paediatricians and dermatologists should screen young people with psoriasis for CVD risk factors. Similarly, Volf et al. 24 highlighted the importance of screening paediatric patients with psoriasis for CVD and MetS risk factors earlier than currently recommended. They suggested the following criteria: triglycerides 100 mg/dl, HDL cholesterol < 50 mg/ dl (female) or < 45 mg/dl (males), fasting blood glucose 110 mg/dl, waist circumference > 75th percentile for age and sex, and systolic or diastolic blood pressure > 90th percentile for age, sex and body weight. 24 Zhu et al. 25 demonstrated that the prevalence of overweight and obesity among patients with psoriasis was significantly higher than in HCs. Overweight/obese paediatric patients with psoriasis were also shown to present with a more severe disease course than similar patients with psoriasis who had normal body weight, even after adjustment for age, sex, family history and duration of psoriasis. Furthermore, the severity of psoriasis (as measured by Psoriasis Area and Severity Index) showed a significant, albeit weak, correlation with patient body mass index (r =0.2, P < 0.05). 25 Currently, preventive cardiovascular therapy is not a standard treatment in patients with psoriasis. However, emerging evidence of metabolic and cardiovascular complications in patients with psoriasis should stimulate discussion about the indications for early protective therapy, especially in patients with metabolic disorders that can lead to potentially lethal complications such as myocardial infarction, stroke and peripheral artery disease. One possible solution that might contribute to early detection of the aforementioned comorbidities is the creation of nationwide registries of patients with juvenile psoriasis. Limitations of the study There were several potential limitations to our study. There was a very limited number of studies that were eligible for the meta-analysis and therefore the results should be interpreted with caution. There was also wide variability of the analysed data within the studies included, which limits the power of the study overall; for example, glucose measurements, although found to be raised in children with psoriasis compared with HCs, were only available for 40 children out of a total of 965 included in the meta-analysis. We tried to overcome these apparent limitations by using the random effects model. Conclusion Decreased levels of HDL cholesterol and increased concentrations of fasting glucose may represent very early stages of MetS in children with psoriasis. However, a large population-based study is needed to establish the relationship between psoriasis and MetS in children, including the environmental, genetic and immunological factors leading to their co-occurrence. References 1 Mabuchi T, Chang TW, Quinter S et al. Chemokine receptors in the pathogenesis and therapy of psoriasis. J Dermatol Sci 2012; 65: Augustin M, Glaeske G, Radtke MA et al. Epidemiology and comorbidity of psoriasis in children. Br J Dermatol 2010; 162: Dauden E, Castaneda S, Suarez C et al. Clinical practice guideline for an integrated approach to comorbidity in patients with psoriasis. J Eur Acad Dermatol Venereol 2013; 27: Torres T, Machado S, Mendonca D et al. Cardiovascular comorbidities in childhood psoriasis. Eur J Dermatol 2014; 24: Toruniowa B, Pietrzak A, Urban J et al. The lipid profile in childhood psoriasis. Pediatr Pol 1994; 2: Koebnick C, Black MH, Smith N et al. The association of psoriasis and elevated blood lipids in overweight and obese children. J Pediatr 2011; 159: Au SC, Goldminz AM, Loo DS et al. Association between pediatric psoriasis and the metabolic syndrome. JAm Acad Dermatol 2012; 66: Jensen P, Zachariae C, Iversen L et al. Cardiovascular risk factors in children and adolescents with psoriasis: a case-control study. Acta Derm Venereol 2014; 94: Goldminz AM, Buzney CD, Kim N et al. Prevalence of the metabolic syndrome in children with psoriatic disease. Pediatr Dermatol 2013; 30: Paller AS, Mercy K, Kwasny MJ et al. Association of pediatric psoriasis severity with excess and central adiposity: an international cross-sectional study. JAMA Dermatol 2013; 149: Clinical and Experimental Dermatology 5

6 11 Alberti KG, Eckel RH, Grundy SM et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 2009; 120: Ryan C, Kirby B. Psoriasis is a systemic disease with multiple cardiovascular and metabolic comorbidities. Dermatol Clin 2015; 33: Kassi E, Pervanidou P, Kaltsas G et al. Metabolic syndrome: definitions and controversies. BMC Med 2011; 9: Steinberger J, Daniels SR, Eckel RH et al. Progress and challenges in metabolic syndrome in children and adolescents: a scientific statement from the American Heart Association Atherosclerosis, Hypertension, and Obesity in the Young Committee of the Council on Cardiovascular Disease in the Young; Council on Cardiovascular Nursing; and Council on Nutrition, Physical Activity, and Metabolism. Circulation 2009; 119: Morrison JA, Friedman LA, Wang P et al. Metabolic syndrome in childhood predicts adult metabolic syndrome and type 2 diabetes mellitus 25 to 30 years later. J Pediatr 2008; 152: Fitzgerald R, Sadlier M, Connolly M et al. Psoriasis and insulin resistance: a review. J Diabetes Res Clin Metab 2014; 3: Reich K. The concept of psoriasis as a systemic inflammation: implications for disease management. J Eur Acad Dermatol Venereol 2012; 2: Gottlieb AB, Dann F, Menter A. Psoriasis and the metabolic syndrome. J Drugs Dermatol 2008; 7: Barter PJ. High density lipoprotein: a therapeutic target in type 2 diabetes. Endocrinol Metab (Seoul) 2013; 28: 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: Wootton CI, Murphy R. Psoriasis in children: should we be worried about comorbidities? Br J Dermatol 2013; 168: Morrison JA, Friedman LA, Gray-McGuire C. Metabolic syndrome in childhood predicts adult cardiovascular disease 25 years later: the Princeton Lipid Research Clinics Follow-up Study. Pediatrics 2007; 120: Matusiewicz D, Koerber A, Schadendorf D et al. Childhood psoriasis an analysis of German health insurance data. Pediatr Dermatol 2014; 31: Volf EM, Levine DE, Michelon MA et al. Assessor-blinded study of the metabolic syndrome and surrogate markers of increased cardiovascular risk in children with moderate-to-severe psoriasis compared with age-matched population of children with warts. J Drugs Dermatol 2011; 10: Zhu KJ, He SM, Zhang C et al. Relationship of the body mass index and childhood psoriasis in a Chinese Han population: a hospital-based study. J Dermatol 2012; 39: Clinical and Experimental Dermatology

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