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Open Access

Peer-reviewed

Research Article

An update on psoriasis and metabolic syndrome: A meta-analysis of observational studies

  • Sanminder Singh,

    Roles Conceptualization, Data curation, Formal analysis, Methodology, Visualization, Writing – original draft, Writing – review & editing

    Affiliation University of California, Davis School of Medicine, Sacramento, California, United States of America

    ⨯
  • Paulina Young,

    Roles Conceptualization, Data curation, Formal analysis, Methodology, Visualization, Writing – original draft

    Affiliation Department of Dermatology, Keck School of Medicine, University of Southern California, Los Angeles, California, United States of America

    ⨯
  • April W. Armstrong

    Roles Conceptualization, Data curation, Formal analysis, Methodology, Project administration, Supervision, Visualization, Writing – original draft, Writing – review & editing

    aprilarmstrong@post.harvard.edu

    Affiliation Department of Dermatology, Keck School of Medicine, University of Southern California, Los Angeles, California, United States of America

    ⨯

Abstract

The relationship between psoriasis and metabolic syndrome is not well understood. Though multiple epidemiologic studies have suggested a link between psoriasis and metabolic syndrome, there is a lack of a comprehensive meta-analysis synthesizing the results of all available observational studies to date. In this meta-analysis, we examined global data on the relationship between psoriasis and odds of metabolic syndrome by searching for studies published between 1946–2016. Specifically, we analyzed the results from 35 observational studies from 20 countries with 1,450,188 total participants, of which 46,714 were psoriasis patients. The pooled odds ratio based on random effects analysis was 2.14 (95% CI 1.84–2.48). Publication bias was present, as evidenced by an Egger test and graphical visualization through a funnel plot (p = 0.001). Based on this comprehensive meta-analysis, psoriasis patients have higher odds of having metabolic syndrome when compared with the general population.

Citation: Singh S, Young P, Armstrong AW (2017) An update on psoriasis and metabolic syndrome: A meta-analysis of observational studies. PLoS ONE 12(7): e0181039. https://doi.org/10.1371/journal.pone.0181039

Editor: Shahrad Taheri, Weill Cornell Medical College in Qatar, QATAR

Received: March 9, 2017; Accepted: June 26, 2017; Published: July 18, 2017

Copyright: © 2017 Singh et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the paper.

Funding: The authors received no specific funding for this work.

Competing interests: No relevant financial conflict of interest is present pertaining to this study. Dr. Armstrong’s other disclosures include serving as an investigator and consultant/advisor to AbbVie, Amgen, Celgene, Janssen, Lilly, Novartis, Regeneron, Pfizer, and Modernizing Medicine. Other authors have no disclosures. This does not alter our adherence to PLOS ONE policies on sharing data and materials.

Introduction

Psoriasis is a chronic, inflammatory skin condition that affects between 2–4% of the general population, with recent estimates suggesting over 125 million patients worldwide [1, 2]. It is associated with a number of comorbidities as well as a high socioeconomic burden [3, 4]. Psoriasis patients also experience a decreased quality of life as a result of this disease [5]. The pathogenesis of psoriasis is currently under active investigation, with studies aiming to identify genetic susceptibility loci for psoriasis in order to detect novel targets for systemic therapy [6–9]. While the exact pathogenesis of psoriasis is not fully understood, basic and translational investigations have led to a renewed understanding of Th-17 and Th-1 pathways involved in the development of psoriasis [10]. Notably, the Th-1 pathway involving dysregulation and activation of Th-1 inflammatory cells is thought to contribute to obesity and insulin resistance, which can increase the risk for cardiovascular disease [11–13].

Population studies have found that patients with psoriasis have increased prevalence of cardiovascular risk factors and elevated risk for developing adverse cardiovascular outcomes [14, 15]. Among these studies, investigators have sought to identify the relationship between psoriasis and metabolic syndrome.

Metabolic syndrome is composed of an assortment of metabolic abnormalities that augment the risk of developing cardiovascular disease. The prevalence of metabolic syndrome is 35% in the United States [16] and has been associated with a significant economic burden [17, 18]. In addition to economic costs, metabolic syndrome is associated with a greater risk of cardiovascular mortality [15, 19]. Specifically, according to NCEP ATP III criteria, metabolic syndrome is diagnosed when a person has at least three of these five conditions: 1) waist circumference 102 cm (40 inches) or greater in men or 88 cm (35 inches) or greater in women; if Asian American, 90 cm (35 inches) or greater in men or 80 cm (32 inches) or greater in women, 2) triglycerides 150 mg/dL or higher (or receiving drug therapy for hypertriglyceridemia), 3) high-density lipoprotein- cholesterol complex (HDL-C) less than 40 mg/dL in men or less than 50 mg/dL in women (or receiving drug therapy for reduced HDL-C), 4) blood pressure 130/85 mm Hg or higher (or receiving drug therapy for hypertension), and 5) fasting glucose 100 mg/dL or greater (or receiving drug therapy for hyperglycemia) [20, 21].

Psoriasis and metabolic syndrome may develop interdependently due to a shared immunopathogenesis involving chronic low-level inflammation mediated by pro-inflammatory cytokines such as IFN-gamma, IL-17, IL-23, and TNF-alpha [14, 22–24]. Additionally, some studies have implicated insulin-like growth factor 1 (IGF-1) as a shared mediator in the keratinocyte proliferation seen in psoriasis and the development of diabetes and hyperlipidemia [25, 26].

Several observational studies have suggested an epidemiological link between psoriasis and metabolic syndrome. There is a lack of comprehensive synthesis of observational data that explores the relationship between these two diseases. To examine whether patients with psoriasis are more likely to have metabolic syndrome, we analyzed data from all available observational studies examining the relationship between psoriasis and metabolic syndrome from 1946–2016.

Materials and methods

To examine the association between metabolic syndrome and psoriasis, we followed PRISMA guidelines to perform a meta-analysis of observational studies identified through our two prior systematic reviews [27, 28] combined with additional studies from a new literature search. The PRISMA checklist is attached (S1 File). For the prior systematic reviews, we used the search terms “Psoriasis” [MeSH] and “Metabolic Syndrome X” [MeSH] to search literature from January 1, 1946 to June 30, 2016. To search for any additional studies published after June 30, 2016, we repeated the search using the same search terms and applied a time restriction for studies published from July 1, 2016 to Jan 1, 2017.

From this updated search of the Medline, Embase, Cochrane Central Register, and Scopus databases, we yielded 1346 references. This was inclusive of 41 references identified through the new search. We applied the following inclusion/exclusion criteria to the 1346 references: human subjects, English language, and observational study design (case-control, cohort, cross-sectional, or nested case-control). Additionally, the studies must have provided prevalence or incidence data on metabolic syndrome in conjunction with psoriasis. The studies must have compared prevalence of metabolic syndrome in healthy or non-psoriasis controls. The diagnosis of psoriasis and metabolic syndrome must be made by a physician and documented in the medical record. Studies evaluating pediatric patients were excluded, as were review articles, commentaries, case reports, case series, and letters to the editor (Fig 1).

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Fig 1. Selection process for studies included in the meta-analysis.

https://doi.org/10.1371/journal.pone.0181039.g001

Once duplicates were removed and initial screening performed by two authors, we performed a full-length review of 115 references and excluded 80 for the following reasons: full-length articles unavailable (n = 12), non-English (n = 5), no non-psoriasis control group (n = 10), included pediatric psoriasis patients (n = 8), case report/commentary/letter (n = 7), did not provide metabolic syndrome prevalence (n = 2), reviews (n = 15), PsA patients only (n = 3), only assessed separate metabolic syndrome components (n = 2), did not measure association between psoriasis and metabolic syndrome (n = 14), did not include percentages or patient numbers (n = 1), and focused on non-human model (n = 1). While there were some case series/reports relevant to this topic, we focused our systematic review and meta-analysis on observational studies. We selected six new references to be systematically reviewed in this paper. For the meta-analysis, we drew upon 29 studies from our previous systematic reviews and added six additional studies from an updated search, for a total of 35 studies to be analyzed.

We extracted prevalence of metabolic syndrome in psoriasis patients versus controls as well as the reported effect size where available, such as odds ratios. Of the 35 studies included in the meta-analysis, 16 reported unadjusted odds ratios, 10 reported adjusted odds ratios, seven studies provided prevalence rates as percent values without calculated odds ratios, and two reported number of patients with metabolic syndrome without percent values or odds ratios. For studies without a published odds ratio value, we calculated unadjusted odds ratios using STATA 14.1 [29]. In studies where investigators provided multiple odds ratios for subsets of psoriasis patients without an overall odds ratio, we used all reported odds ratios for the meta-analysis [30, 31].

Using odds ratio data obtained from the published results, we estimated the pooled odds ratio for the presence of metabolic syndrome in psoriasis patients. To account for any study heterogeneity, we utilized the random-effects model of DerSimonian and Laird [32].

We performed an Egger’s regression test to assess for publication bias. Publication bias may arise when studies with statistically significant results are more likely to be published and cited, and are preferentially published in English language journals [33]. Studies that do not suggest a relationship between psoriasis and metabolic syndrome may be less likely to get published, thus this Egger’s regression test enables us to assess the degree of publication bias in this field of investigation. Specifically, we graphically represented the estimate of effect from each study in the meta-analysis against a measure of its precision, producing a funnel plot, and a bias coefficient was calculated to confirm the findings of the funnel plot. We also examined between-study heterogeneity using the I2 statistic.

All analyses were performed using STATA Version 14.1 (STATA Corp LP, College Station, TX).

Results

This meta-analysis analyzed data from 35 studies with a total of 1,450,188 participants, among which 46,714 were patients with psoriasis. We searched over 70 years of literature, spanning from January 1, 1946 to Jan 1, 2017, using the Medline, Embase, Cochrane Central register, and Scopus databases [27, 28]. Out of the 35 articles, ten provided adjusted odds ratios after multivariate adjustment for factors such as age, sex, smoking, alcohol consumption, physical activity, and education [31, 34–42]. Among the remaining articles, 16 provided unadjusted odds ratios [30, 43–58], seven provided percent values for metabolic syndrome prevalence [59–65], and two provided specific numbers of patients affected without percent values or odds ratios. For the nine articles that did not provide any odds ratios, we calculated unadjusted odds that were then included in the meta-analysis (Table 1).

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Table 1. Study characteristics and outcomes for psoriasis and metabolic syndrome.

https://doi.org/10.1371/journal.pone.0181039.t001

All of the studies included in this meta-analysis reported the prevalence of metabolic syndrome in psoriasis patients versus non-psoriasis controls. With the inclusion of seven new studies published from July 1, 2016- January 1, 2017, the unadjusted odds ratios for metabolic syndrome in psoriasis patients ranged from 0.84–6.09, and the adjusted odds ratios ranged from 1.22–5.14. When stratified by disease severity, the prevalence of metabolic syndrome demonstrated a dose-dependent relationship with the degree of psoriasis severity [30, 37, 40, 56, 61, 62, 68]. For example, the adjusted odds ratio for metabolic syndrome in severe psoriasis was 1.98, while in mild psoriasis it was 1.22 [37]. For the meta-analysis, we utilized random effects analysis to calculate the pooled odds ratio of 2.14 (95% CI 1.84–2.48), as shown in Fig 2.

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Fig 2. Prevalence of metabolic syndrome in psoriasis patients.

This is a forest plot examining observational studies. The diamond represents the exact estimate from the study. The width of the line extending from each diamond represents the 95% confidence interval (CI). OR, odds ratio; MetSyn, Metablic syndrome.

https://doi.org/10.1371/journal.pone.0181039.g002

To assess publication bias, we examined a funnel plot and performed an Egger test to determine a bias coefficient (Fig 3). The funnel plot revealed asymmetry, suggesting publication bias, and the Egger test confirmed bias (P = 0.001). I2 value of 83.2% (p = 0.000) suggests presence of between-study heterogeneity.

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Fig 3. Funnel plot of included studies.

https://doi.org/10.1371/journal.pone.0181039.g003

Discussion

This is a meta-analysis based on primary studies published between 1946–2017 that were identified through a comprehensive systematic review. The meta-analysis examines the relationship between psoriasis and metabolic syndrome, incorporating 35 articles from 20 countries with a total of 1,450,188 participants, including 46,714 psoriasis patients. To our knowledge, this is the most comprehensive meta-analysis on psoriasis and metabolic syndrome to date. Our pooled OR of 2.14 indicates a higher prevalence of metabolic syndrome in psoriasis patients in comparison to the general population. With the added impact of new and previously unexamined primary studies, our study maintains and strengthens the positive correlation between psoriasis and metabolic syndrome found in our 2013 meta-analysis, which had demonstrated a pooled odds ratio of 2.26 from 12 studies [27, 28].

Metabolic syndrome encompasses a group of cardiovascular risk factors that overlap with psoriasis in both pathogenesis and outcome. These include abdominal obesity, hypertension, dyslipidemia, and insulin resistance. Additionally, metabolic syndrome, along with several of its components when considered individually, increase in prevalence along with psoriasis disease severity [69].

Shared underlying mechanisms between psoriasis and metabolic syndrome have been proposed. One such theory centers on how the chronic inflammation in psoriasis also contributes to insulin resistance and endothelial cell dysfunction in atherosclerosis. This inflammatory cascade ultimately culminates in adverse cardiovascular events such as myocardial infarction or stroke [70].

Specifically, psoriasis and metabolic syndrome display similar inflammatory profiles with Th1 and Th17 T-cells as well as overexpression of cytokines such as IL-6 and TNF-alpha [69]. For example, TNF-alpha, which is overexpressed in patients with psoriasis, is also elevated with abdominal obesity, a component of metabolic syndrome. It induces the production of adhesion molecules by endothelial cells, promoting monocyte binding in the early phases of atherosclerosis [71]. If left uncontrolled, the immunologic mediators common to both disease processes may lead to cardiovascular impairment or death.

The results of the meta-analysis need to be interpreted in the context of the primary articles. One factor to consider in examining any meta-analysis is sources of heterogeneity. Heterogeneity can increase generalizability of the study findings, but it can also impact interpretation of the association between exposure and outcome. Aside from differences in study location, setting, and design, some studies reported unadjusted odds ratios while others reported adjusted odds ratios. Furthermore, the assessment of metabolic syndrome varied as well, with some studies using NCEP-ATP III criteria, while others using the South Asian Modified version of the NCEP-ATP III criteria or the International Diabetes Foundation (IDF) definition [72]. Therefore, we used random effects analysis to account for these sources of heterogeneity, and the odds of metabolic syndrome in psoriasis patients remained more than twice that of the general population.

As with most meta-analyses, in this meta-analysis, we detected publication bias through use of the Egger test. Therefore, the results of this study may reflect a slight overestimate of the frequency of metabolic syndrome in psoriasis patients. Nevertheless, the outcomes of a vast majority of the 35 studies evaluated suggest a positive and strong correlation between psoriasis and metabolic syndrome.

Through a thorough evaluation of existing literature, we found significantly increased odds of metabolic syndrome in the psoriasis population compared to non-psoriasis controls. We also found there to be a dose-dependent relationship between psoriasis disease severity and metabolic syndrome prevalence. Psoriasis is a systemic disease with significant morbidity and mortality. This study emphasizes the critical need for providers to screen psoriasis patients for cardiometabolic diseases and provide structured management. This may require dermatologists to work in concert with primary care providers and other specialists to coordinate care for psoriasis and its comorbidities. Finally, the exact pathologic mechanisms shared by these two disease processes, as well as the directionality of the relationship, are not well understand and need to be elucidated through further translational work. Future translational discoveries may guide the development of new treatments or the refined application of existing therapies for both psoriasis and metabolic syndrome.

Supporting information

S1 File. PRISMA checklist.

https://doi.org/10.1371/journal.pone.0181039.s001

(PDF)

Acknowledgments

We would like to thank Dr. Wendy Mack for her assistance with the statistical aspects of this meta-analysis.

References

  1. 1. Parisi R, Symmons DPM, Griffiths CEM, Ashcroft DM, Management I. Global Epidemiology of Psoriasis: A Systematic Review of Incidence and Prevalence. J Invest Dermatol. 2013;133(2):377–85. pmid:23014338
  2. 2. Rachakonda TD, Schupp CW, Armstrong AW. Psoriasis prevalence among adults in the United States. J Am Acad Dermatol. 2014;70(3):512–6. pmid:24388724
  3. 3. van der Voort EAM, Koehler EM, Dowlatshahi EA, Hofman A, Stricker BH, Janssen HLA, et al. Psoriasis is independently associated with nonalcoholic fatty liver disease in patients 55 years old or older: Results from a population-based study. J Am Acad Dermatol. 2014;70(3):517–24. pmid:24373781
  4. 4. Yeung H, Takeshita J, Mehta NN, Kimmel SE, Ogdie A, Margolis DJ, et al. Psoriasis Severity and the Prevalence of Major Medical Comorbidity A Population-Based Study. Jama Dermatol. 2013;149(10):1173–9. pmid:23925466
  5. 5. Stern RS, Nijsten T, Feldman SR, Margolis DJ, Rolstad T. Psoriasis is common, carries a substantial burden even when not extensive, and is associated with widespread treatment dissatisfaction. The journal of investigative dermatology Symposium proceedings. 2004;9(2):136–9. pmid:15083780
  6. 6. Elder JT, Bruce AT, Gudjonsson JE, Johnston A, Stuart PE, Tejasvi T, et al. Molecular Dissection of Psoriasis: Integrating Genetics and Biology. J Invest Dermatol. 2010;130(5):1213–26. pmid:19812592
  7. 7. Hawkes JE, Nguyen GH, Fujita M, Florell SR, Callis Duffin K, Krueger GG, et al. microRNAs in Psoriasis. J Invest Dermatol. 2016;136(2):365–71. pmid:26802234
  8. 8. Winge MCC, Ohyama B, Dey CN, Boxer LM, Li W, Ehsani-Chimeh N, et al. RAC1 activation drives pathologic interactions between the epidermis and immune cells. J Clin Invest. 2016;126(7):2661–77. pmid:27294528
  9. 9. Wippel-Slupetzky K, Stingl G. Future perspectives in the treatment of psoriasis. Curr Probl Dermatol. 2009;38:172–89. pmid:19710556
  10. 10. Golden JB, McCormick TS, Ward NL. IL-17 in psoriasis: Implications for therapy and cardiovascular co-morbidities. Cytokine. 2013;62(2):195–201. pmid:23562549
  11. 11. Shiba M, Kato T, Funasako M, Nakane E, Miyamoto S, Izumi T, et al. Association between Psoriasis Vulgaris and Coronary Heart Disease in a Hospital-Based Population in Japan (vol 11, e0149316, 2016). Plos One. 2016;11(6).
  12. 12. Winer S, Chan Y, Paltser G, Truong D, Tsui H, Bahrami J, et al. Normalization of Obesity-Associated Insulin Resistance through Immunotherapy: CD4+ T Cells Control Glucose Homeostasis. Nature medicine. 2009;15(8):921–9. pmid:19633657
  13. 13. Wu JJ, Poon KYT, Channual JC, Shen AYJ. Association Between Tumor Necrosis Factor Inhibitor Therapy and Myocardial Infarction Risk in Patients With Psoriasis. Arch Dermatol. 2012;148(11):1244–50. pmid:22911151
  14. 14. Armstrong EJ, Harskamp CT, Armstrong AW. Psoriasis and major adverse cardiovascular events: a systematic review and meta-analysis of observational studies. J Am Heart Assoc. 2013;2(2):e000062. pmid:23557749
  15. 15. Gelfand JM, Neimann AL, Shin DB, Wang X, Margolis DJ, Troxel AB. Risk of myocardial infarction in patients with psoriasis. JAMA. 2006;296(14):1735–41. pmid:17032986
  16. 16. Aguilar M, Bhuket T, Torres S, Liu B, Wong RJ. Prevalence of the metabolic syndrome in the United States, 2003–2012. JAMA. 2015;313(19):1973–4. pmid:25988468
  17. 17. Scholze J, Alegria E, Ferri C, Langham S, Stevens W, Jeffries D, et al. Epidemiological and economic burden of metabolic syndrome and its consequences in patients with hypertension in Germany, Spain and Italy; a prevalence-based model. BMC Public Health. 2010;10:529. pmid:20813031
  18. 18. Sullivan PW, Ghushchyan V, Wyatt HR, Hill JO. The medical cost of cardiometabolic risk factor clusters in the United States. Obesity (Silver Spring). 2007;15(12):3150–8.
  19. 19. Isomaa B, Almgren P, Tuomi T, Forsen B, Lahti K, Nissen M, et al. Cardiovascular morbidity and mortality associated with the metabolic syndrome. Diabetes Care. 2001;24(4):683–9. pmid:11315831
  20. 20. Expert Panel on Detection E, Treatment of High Blood Cholesterol in A. 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(19):2486–97. pmid:11368702
  21. 21. Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, et al. Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation. 2005;112(17):2735–52. pmid:16157765
  22. 22. Esser N, Legrand-Poels S, Piette J, Scheen AJ, Paquot N. Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res Clin Pr. 2014;105(2):141–50.
  23. 23. Moon YS, Kim DH, Song DK. Serum tumor necrosis factor-alpha levels and components of the metabolic syndrome in obese adolescents. Metabolism. 2004;53(7):863–7. pmid:15254878
  24. 24. Popa C, Netea MG, van Riel PL, van der Meer JW, Stalenhoef AF. The role of TNF-alpha in chronic inflammatory conditions, intermediary metabolism, and cardiovascular risk. J Lipid Res. 2007;48(4):751–62. pmid:17202130
  25. 25. Azfar RS, Gelfand JM. Psoriasis and metabolic disease: epidemiology and pathophysiology. Curr Opin Rheumatol. 2008;20(4):416–22. pmid:18525354
  26. 26. Yoo H, Kim SJ, Kim Y, Lee H, Kim TY. Insulin-like growth factor-II regulates the 12-lipoxygenase gene expression and promotes cell proliferation in human keratinocytes via the extracellular regulatory kinase and phosphatidylinositol 3-kinase pathways. Int J Biochem Cell B. 2007;39(6):1248–59.
  27. 27. Armstrong AW, Harskamp CT, Armstrong EJ. Psoriasis and metabolic syndrome: a systematic review and meta-analysis of observational studies. J Am Acad Dermatol. 2013;68(4):654–62. pmid:23360868
  28. 28. Singh S, Young P, Armstrong AW. Relationship between psoriasis and metabolic syndrome: a systematic review. G Ital Dermatol Venereol. 2016;151(6):663–77. pmid:27589483
  29. 29. Szumilas M. Explaining odds ratios. J Can Acad Child Adolesc Psychiatry. 2010;19(3):227–9. pmid:20842279
  30. 30. Al-Mutairi N, Al-Farag S, Al-Mutairi A, Al-Shiltawy M. Comorbidities associated with psoriasis: an experience from the Middle East. Journal of Dermatology. 2010;37(2):146–55. pmid:20175849
  31. 31. Miller IM, Ellervik C, Zarchi K, Ibler KS, Vinding GR, Knudsen KM, et al. The association of metabolic syndrome and psoriasis: a population- and hospital-based cross-sectional study. Journal of the European Academy of Dermatology & Venereology. 2015;29(3):490–7.
  32. 32. Brockwell SE, Gordon IR. A comparison of statistical methods for meta-analysis. Stat Med. 2001;20(6):825–40. pmid:11252006
  33. 33. Juni P, Holenstein F, Sterne J, Bartlett C, Egger M. Direction and impact of language bias in meta-analyses of controlled trials: empirical study. Int J Epidemiol. 2002;31(1):115–23. pmid:11914306
  34. 34. Danielsen K, Wilsgaard T, Olsen AO, Eggen AE, Olsen K, Cassano PA, et al. Elevated odds of metabolic syndrome in psoriasis: a population-based study of age and sex differences. British Journal of Dermatology. 2015;172(2):419–27. pmid:25059341
  35. 35. Itani S, Arabi A, Harb D, Hamzeh D, Kibbi AG. High prevalence of metabolic syndrome in patients with psoriasis in Lebanon: a prospective study. Int J Dermatol. 2016;55(4):390–5. pmid:26748974
  36. 36. Kokpol C, Aekplakorn W, Rajatanavin N. Prevalence and characteristics of metabolic syndrome in South-East Asian psoriatic patients: a case-control study. Journal of Dermatology. 2014;41(10):898–902. pmid:25201476
  37. 37. Langan SM, Seminara NM, Shin DB, Troxel AB, Kimmel SE, Mehta NN, et al. Prevalence of metabolic syndrome in patients with psoriasis: a population-based study in the United Kingdom. Journal of Investigative Dermatology. 2012;132(3 Pt 1):556–62. pmid:22113483
  38. 38. Love TJ, Qureshi AA, Karlson EW, Gelfand JM, Choi HK. Prevalence of the metabolic syndrome in psoriasis: results from the National Health and Nutrition Examination Survey, 2003–2006. Archives of Dermatology. 2011;147(4):419–24. pmid:21173301
  39. 39. Mebazaa A, El Asmi M, Zidi W, Zayani Y, Cheikh Rouhou R, El Ounifi S, et al. Metabolic syndrome in Tunisian psoriatic patients: prevalence and determinants. Journal of the European Academy of Dermatology & Venereology. 2011;25(6):705–9.
  40. 40. Parodi A, Aste N, Calvieri C, Cantoresi F, Carlesimo M, Fabbri P, et al. Metabolic syndrome prevalence in psoriasis: a cross-sectional study in the Italian population. American Journal of Clinical Dermatology. 2014;15(4):371–7. pmid:24756247
  41. 41. Vaya A, Ricart JM, Andino B, Todoli J, Nunez C, Calvo J, et al. Psoriasis and hemorheology. Influence of the metabolic syndrome. Clinical Hemorheology & Microcirculation. 2013;55(3):331–9.
  42. 42. Djurović MR, Janković J, Janković S. Prevalence of metabolic syndrome in montenegrin patients with psoriasis. Vojnosanitetski Pregled. 2016;73(11):1016–21.
  43. 43. Arias-Santiago S, Orgaz-Molina J, Castellote-Caballero L, Arrabal-Polo MA, Garcia-Rodriguez S, Perandres-Lopez R, et al. Atheroma plaque, metabolic syndrome and inflammation in patients with psoriasis. European Journal of Dermatology. 2012;22(3):337–44. pmid:22503884
  44. 44. Augustin M, Reich K, Glaeske G, Schaefer I, Radtke M. Co-morbidity and age-related prevalence of psoriasis: Analysis of health insurance data in Germany. Acta Dermato-Venereologica. 2010;90(2):147–51. pmid:20169297
  45. 45. Bongiorno MR, Doukaki S, Rizzo D, Arico M. The prevalence of the obesity in patients with moderate to severe psoriasis in Sicily populations. J Eur Acad Dermatol Venereol. 2010;24(1):92–3. pmid:19496896
  46. 46. Chen YJ, Shen JL, Wu CY, Chang YT, Chen CM, Lee FY. Elevated plasma osteopontin level is associated with occurrence of psoriasis and is an unfavorable cardiovascular risk factor in patients with psoriasis. J Am Acad Dermatol. 2009;60(2):225–30. pmid:19028408
  47. 47. Chen YJ, Wu CY, Shen JL, Chu SY, Chen CK, Chang YT, et al. Psoriasis independently associated with hyperleptinemia contributing to metabolic syndrome. Archives of Dermatology. 2008;144(12):1571–5. pmid:19075139
  48. 48. Damevska K, Neloska L, Gocev G, Mihova M. Metabolic syndrome in untreated patients with psoriasis: case-control study. Journal der Deutschen Dermatologischen Gesellschaft. 2013;11(12):1169–75. pmid:24267013
  49. 49. Gisondi P, Tessari G, Conti A, Piaserico S, Schianchi S, Peserico A, et al. Prevalence of metabolic syndrome in patients with psoriasis: a hospital-based case-control study. British Journal of Dermatology. 2007;157(1):68–73. pmid:17553036
  50. 50. Irimie M, Oanţă A, Irimie CA, Fekete LG, Minea DI, Pascu A. Cardiovascular risk factors in patients with chronic plaque psoriasis: A case-control study on the brasov county population. Acta Dermatovenerologica Croatica. 2015;23(1):28–35. pmid:25969910
  51. 51. Nisa N, Qazi MA. Prevalence of metabolic syndrome in patients with psoriasis. Indian Journal of Dermatology, Venereology & Leprology. 2010;76(6):662–5.
  52. 52. Praveenkumar U, Ganguly S, Ray L, Nanda SK, Kuruvila S. Prevalence of Metabolic Syndrome in Psoriasis Patients and its Relation to Disease Duration: A Hospital Based Case-Control Study. J Clin Diagn Res. 2016;10(2):WC01–5. pmid:27042565
  53. 53. Sharma YK, Prakash N, Gupta A. Prevalence of metabolic syndrome as per the NCEP and IDF definitions vis-a-vis severity and duration of psoriasis in a semi-urban Maharashtrian population: A case control study. Diabetes and Metabolic Syndrome: Clinical Research and Reviews. 2016.
  54. 54. Sommer DM, Jenisch S, Suchan M, Christophers E, Weichenthal M. Increased prevalence of the metabolic syndrome in patients with moderate to severe psoriasis. Archives of Dermatological Research. 2006;298(7):321–8. pmid:17021763
  55. 55. Takahashi H, Takahashi I, Honma M, Ishida-Yamamoto A, Iizuka H. Prevalence of metabolic syndrome in Japanese psoriasis patients. Journal of Dermatological Science. 2010;57(2):143–4. pmid:20005080
  56. 56. Zindanci I, Albayrak O, Kavala M, Kocaturk E, Can B, Sudogan S, et al. Prevalence of metabolic syndrome in patients with psoriasis. Thescientificworldjournal. 2012;2012:312463. pmid:22654590
  57. 57. Lai YC, Yew YW. Psoriasis as an Independent Risk Factor for Cardiovascular Disease: An Epidemiologic Analysis Using a National Database. Journal of Cutaneous Medicine and Surgery. 2016;20(4):327–33. pmid:26316538
  58. 58. Kothiwala SK, Khanna N, Tandon N, Naik N, Sharma VK, Sharma S, et al. Prevalence of metabolic syndrome and cardiovascular changes in patients with chronic plaque psoriasis and their correlation with disease severity: A hospital-based cross-sectional study. Indian Journal of Dermatology, Venereology and Leprology. 2016;82(5):510–8. pmid:27297282
  59. 59. Akcali C, Buyukcelik B, Kirtak N, Inaloz S. Clinical and laboratory parameters associated with metabolic syndrome in Turkish patients with psoriasis. Journal of International Medical Research. 2014;42(2):386–94. pmid:24445696
  60. 60. Balci A, Balci DD, Yonden Z, Korkmaz I, Yenin JZ, Celik E, et al. Increased amount of visceral fat in patients with psoriasis contributes to metabolic syndrome. Dermatology. 2010;220(1):32–7. pmid:19887761
  61. 61. Karoli R, Fatima J, Shukla V, Dhillon KS, Khanduri S, Maini S, et al. A study of cardio-metabolic risk profile in patients with psoriasis. Journal of the Association of Physicians of India. 2013;61(11):798–803. pmid:24974491
  62. 62. 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 Journal of Dermatology. 2012;57(5):353–7. pmid:23112353
  63. 63. Tasliyurt T, Bilir Y, Sahin S, Seckin HY, Kaya SU, Sivgin H, et al. Erectile dysfunction in patients with psoriasis: potential impact of the metabolic syndrome. European Review for Medical & Pharmacological Sciences. 2014;18(4):581–6.
  64. 64. Barrea L, Macchia PE, Di Somma C, Napolitano M, Balato A, Falco A, et al. Bioelectrical phase angle and psoriasis: A novel association with psoriasis severity, quality of life and metabolic syndrome. Journal of Translational Medicine. 2016;14(1).
  65. 65. Vandervoort EAM, Koehler EM, Nijsten T, Stricker BH, Hofman A, Janssen HLA, et al. Increased prevalence of advanced liver fibrosis in patients with psoriasis: A cross-sectional analysis from the rotterdam study. Acta Derm-Venereol. 2016;96(2):213–7. pmid:26062958
  66. 66. Brito-Luna MJ, Villanueva-Quintero DG, Sandoval-Talamantes AK, Fafutis-Morris M, Graciano-Machuca O, Sanchez-Hernandez PE, et al. Correlation of IL-12, IL-22, and IL-23 in patients with psoriasis and metabolic syndrome. Preliminary report. Cytokine. 2016;85:130–6. pmid:27344023
  67. 67. Lai YC, Yew YW. Psoriasis and uric acid: A population-based cross-sectional study. Clin Exp Dermatol. 2016;41(3):260–6. pmid:26643816
  68. 68. Itani S, Arabi A, Harb D, Hamzeh D, Kibbi AG. High prevalence of metabolic syndrome in patients with psoriasis in Lebanon: A prospective study. International Journal of Dermatology. 2016;55(4):390–5. pmid:26748974
  69. 69. Gelfand JM, Yeung H. Metabolic Syndrome in Patients with Psoriatic Disease. J Rheumatol. 2012;39:24–8.
  70. 70. Boehncke WH, Boehncke S, Tobin AM, Kirby B. The 'psoriatic march': a concept of how severe psoriasis may drive cardiovascular comorbidity. Experimental Dermatology. 2011;20(4):303–7. pmid:21410760
  71. 71. Liakou AI Z C. Links and risks associated with psoriasis and metabolic syndrome. Psoriasis: Targets and Therapy. 2015;November 2015(5):4.
  72. 72. Parikh RM, Mohan V. Changing definitions of metabolic syndrome. Indian J Endocrinol Metab. 2012;16(1):7–12. pmid:22276247