The Linkage between Psoriasis and Non-alcoholic Fatty Liver Disease: a Literature Review
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1 2014;22(2): CLINICAL ARTICLE The Linkage between Psoriasis and Non-alcoholic Fatty Liver Disease: a Literature Review Andréia Nogueira Ramos, Bruno de Oliveira Rocha, Vitória Regina Pedreira de Almeida Rêgo, Ivonise Follador, Maria de Fátima Santos Paim de Oliveira Department of Dermatology, Federal University of Bahia, Salvador, Bahia, Brazil Corresponding author: Maria de Fátima Santos Paim de Oliveira, MD, MSc, PhD Artesão João da Prata Street, 267, Room 602, Itaigara, Salvador Bahia Brazil mfatimapaim@gmail.com SUMMARY Psoriasis is a chronic systemic inflammatory disease mainly affecting the skin. Population-based surveys have shown a higher prevalence of non-alcoholic fat liver disease (NAFLD) in patients with psoriasis compared with the general population, especially in those with a greater psoriasis area and severity index (PASI). It is speculated that similar pathogenic bases may play a role in this association, highlighting insulin resistance and the release of inflammatory cytokines as the most likely causes. In the present work, we review basic aspects of the relationship between psoriasis and NAFLD. Key words: psoriasis, non-alcoholic fatty liver disease, steatohepatitis Received: May 20, 2013 Accepted: November 18, 2013 Introduction Psoriasis is a chronic systemic inflammatory disease mainly affecting the skin (1-7). Its worldwide estimated prevalence is around 2-3%, with no gender preference, but influenced by ethnic factors since this prevalence among blacks is 0 to 0.7% (1.2). The pathogenesis of psoriasis is not completely understood, but it is known that genetic, environmental, and immunological factors are involved (2-6,8). Epidemiological studies suggest that several genes are probably involved in the pathogenesis of psoriasis (1-5). The risk of a child to develop psoriasis if both parents are affected is estimated to be 40%, 15% if only one parent is affected, and 6% if a sibling is affected (3). A locus of particular importance, related to 50% of psoriasis cases, is located in region 1 of the Major Histocompatibility Complex (MHC) in chromosome 6 PSORS1 ( Psoriais Suceptibility ) (2). Some authors, however, believe that it could just be a regulatory variant in this region (4). Other less important loci are located on chromosomes 17q25 (PSORS2), 4q34 (PSORS3), 1q (PSORS4), 3q21 (PSORS5), 19p13 (PSORS6), and 1p (PSORS7). The MHC alleles most involved in psoriasis are HLA-B13, HLA-B17, HLA-Bw57, and HLACw6 (2). Nevertheless, psoriasis can still be triggered or exacerbated by environmental factors, such as the use of certain drugs (β-blockers, lithium, non-steroidal anti-inflammatory, and anti-malarial compounds), infections, alcohol consumption, and smoking habits (2,4,5). Two main types of cells interact in the formation of the psoriatic lesion: epidermal keratinocytes and mononuclear leukocytes. Cytokines produced by epidermal keratinocytes act on the innate and acquired immune system by stimulating dendritic cells, neutrophils, and T-cells. Additionally, they regulate the 132
2 expression of genes, generate regenerative hyperplasia, and induce the expression of adhesion molecules (4). The T-cells, predominantly Th1, Th17 and Th22, in turn act through the production of cytokines (mainly IFN-γ, IL-2, IL-17, IL-22), which induces keratinocyte proliferation (4,8). The release of these cytokines allows expression of endothelial adhesion molecules (ICAM-1, VCAM-1, and E-selectin) that promote leukocyte migration through the dermal matrix toward the epidermis, with extravasation of leukocytes at the site of inflammation (2). The dendritic cells, another group of effector cells of the innate immune response in psoriasis, can act causing the release of cytokines (mainly IL-23 and IL-20), which will activate T-cells and keratinocytes or act in their usual function of antigenpresenting cells, helping to trigger the acquired immune response (4,6). Psoriasis, especially the most severe variants, has been associated with certain systemic diseases with which it has similar pathogenic factors, albeit a distinct target organ (2,3,5,6,9,10). Related diseases include arthritis, inflammatory bowel disease, uveitis, and psychiatric disorders. In this context, recent researches have linked psoriasis to metabolic syndrome and to its components separately (central obesity, atherogenic dyslipidemia, insulin resistance, and high blood pressure) (2). The association between psoriasis and its comorbidities is most likely to be explained by the chronic state of systemic inflammation (3,6,11). Cases of fatty liver disease with inflammation that resembled the alcoholic steatohepatitis but with the absence of alcohol intake were described about 30 years ago in Japan and later in the US. The term nonalcoholic steatohepatitis (NASH) was coined in 1980 to designate fatty liver disease (12). However, steatosis is defined as the presence of at least 5% of hepatocytes containing fat droplets, while steatohepatitis is associated with inflammation and hepatocellular injury with or without fibrosis (11,13,14). Hence, the term NASH was later expanded to nonalcoholic fatty liver disease (NAFLD), to encompass the whole disease spectrum Figure 1 (12). The NAFLD is a leading cause of elevated liver enzymes and the most prevalent form of liver disease in developed countries (9,12). It is a clinicopathological syndrome which covers everything from a simple steatosis to a steatohepatitis, fibrosis, and cirrhosis (12), and is characterized by focal or diffuse accumulation of fat in the liver parenchyma in patients with no history of alcohol consumption (12,15). Less commonly, NAFLD may be the result of secondary causes such as medications (corticosteroids, methotrexate, amiodarone, and tamoxifen), nutritional causes (rapid weight loss, acute inanition, and total parenteral nutrition), metabolic diseases (with lipodystrophy or dysbetalipoproteinemia), and abdominal surgery (bile-digestive derivations and extensive small intestine resection). There are also reports of its association with the hepatitis C virus (HCV), human immunodeficiency virus (HIV), and polycystic ovary syndrome (13,16). NAFLD is very common in the general population, and can affect any age and ethnic group. Although its prevalence is estimated to be around 33%, there is controversy regarding the precision of the data and sensitivity/specificity of the diagnostic methods used in the surveys (16). When compared with lean subjects, obese patients are more likely to present with NAFLD (16% vs. 76%) (12). Extrapolating the results from studies that include liver biopsies and necropsies, between 2-7% of the general population may have nonalcoholic steatohepatitis and fibrosis or cirrhosis, which may reach Figure 1. The spectrum and natural history of nonalcoholic fatty liver disease (NAFLD). 133
3 Figure 2. Risk factors and their relationship with psoriasis and nonalcoholic fatty liver disease (NAFLD). 20% in obese subjects (12). The overall prevalence in children is 2.6%, but increases to more than 53% in obese children. In Brazil, a study found NAFLD in 35% of the subjects, predominantly older people (15). Risk factors for developing NAFLD include central obesity, insulin resistance, type 2 diabetes mellitus, and hyperlipidemia, which is why it is being considered a liver manifestation of metabolic syndrome (9,13,16,17). Despite this, only recently has the significance of NAFLD been recognized and studied. It was found that, while patients with only steatosis have a life expectancy similar to the general population and a low risk of developing end-stage liver disease, those with steatohepatitis have a 37% higher risk for progressing to fibrosis in a period of 3.2 years if presenting a high body mass index (BMI) and diabetes. In addition, deaths from liver or cardiovascular diseases are also higher in patients with NAFLD (9). Table 1. Cytokine profile in psoriasis and nonalcoholic fatty liver disease (NAFLD). Adiponectin Leptin TNFα IL-1 IL-6 Psoriasis NAFLD The pathogenesis of NAFLD is not yet completely understood, but the main hypothesis takes into account an increased consumption of fatty foods and the accumulation of fat in the liver due to insulin resistance (15,16). The genetics of NAFLD are not well understood and, although genes that are implicated in its development have recently been identified, more studies are needed to determine whether these findings can be verified. The genes that influence the etiologic factors which have a causal relationship with the disease (e.g.: insulin resistance/obesity) should also be considered. More than behavioral factors, they are at least partially genetically determined. It is likely that this is the point of connection of NAFLD with psoriasis (18). The management of NAFLD includes reduction of BMI and recovery of insulin sensitivity, since there are still no approved drugs for its treatment (9). Psoriasis and NAFLD: chronic conditions of inflammation and insulin resistance The first report of patients with psoriasis and concomitant hepatic steatosis was unexpectedly found during a survey which aimed to evaluate patients with NAFLD. These patients presented with liver abnormalities seen on ultrasonography and underwent a liver biopsy, which revealed hepatic fibrosis (19). 19 Afterwards, population-based surveys have shown a higher prevalence of NAFLD in patients with psoriasis compared with the general population. It was also observed that the psoriasis area and severity index (PASI) was higher in patients with both psoriasis and NAFLD than in those with psoriasis only. These publications raised the possibility that the 134
4 relationship between psoriasis and NAFLD is due to similar pathogenic bases (Figure 2), especially insulin resistance and the release of inflammatory cytokines (Table 1) (11,13,20). As NAFLD began to be considered a part of the metabolic syndrome spectrum, the relationship between NAFLD and psoriasis became grounded in their association with metabolic syndrome (11,13,20,21). Proinflammatory cytokines excessively produced in patients with psoriasis may contribute to the development of insulin resistance, generating lipid abnormalities and culminate in the development of NAFLD. Another important factor in the development of inflammation, insulin resistance, and NAFLD is visceral adipose tissue that releases several free fatty acids, hormones, and adipokines (11). Furthermore, literature data also suggest that this association is even greater in patients with more severe psoriasis and in patients with psoriatic arthritis, once the pathogenesis of psoriasis and psoriatic arthritis is strongly linked to high levels of tumor necrosis factor α (TNFα) (2,4,5,7,8,22), which also play an important role in the pathogenesis of fatty liver disease (7,22,23). It should be noted that the progression of NAFLD to NASH is at least partly associated with an increased TNFα/adiponectin levels ratio (23). Adiponectin is an adipocyte-specific secretory protein with anti-inflammatory and anti-diabetic properties (23). Low levels of adiponectin are found in cases of hyperinsulinemia, obesity, type II diabetes, and, being related to an increased probability of cardiovascular events, also in patients with moderate to severe psoriasis (10). Interleukin-6 (IL-6) increases the production of C-reactive protein (CRP) by the liver and can alter insulin sensitivity, along with TNFα(23). In a recently published clinical trial, it was noted that anti-tnfα drugs seems to prevent hepatic fibrosis in patients with psoriasis, and that this effect could be related to its anti-inflammatory and glucose homeostatic effects. In the same survey, the patients with more severe insulin resistance (assessed by fasting insulin levels and homeostasis model assessment HOMA) were also more likely to develop hepatic fibrosis (22). A study by Gisondi et al. posited that NAFLD may contribute to the worsening of the psoriasis by releasing pathogenic mediators from the inflamed liver, including reactive oxygen species, increased levels of CRP, and IL-6, which would also be mediators of atherogenesis that is associated with liver damage (11). Miele et al. also observed that patients with both psoriasis and NAFLD are at a greater risk of developing severe liver disease (steatohepatitis and fibrosis) than those with NAFLD but without psoriasis (23). Despite all this evidence, the fact that the pathogenesis of neither psoriasis nor NAFLD is fully understood prevents us from establishing the exact pathophysiological and genetic processes involved in the relationship between these two diseases (24). Finally, current literature suggests that patients with both NAFLD and psoriasis have a higher risk of presenting with metabolic syndrome, increased severity of skin and liver diseases, and increased risk of cardiovascular events (11).Thus, early recognition of NAFLD by radiological imaging tests in psoriasis patients is warranted, since it may influence the prognosis and management of the patient as a whole (7,11,20,25). It is noteworthy that the studies presented here used ultrasonography as a diagnostic method for NAFLD, which is more sensitive than liver biopsy for liver fibrosis. Hence, the prevalence of liver fibrosis may have been overestimated in those patients (23). Conclusion NAFLD, currently regarded as a manifestation of metabolic syndrome, is highly prevalent in patients with psoriasis. Taking into account the prognosis of these patients, it is advisable to screen for this disease in patients with psoriasis, especially those who have more severe forms, high BMI, diabetes, and who are scheduled to use potentially hepatotoxic drugs. As the presence of comorbid conditions has important implications in the global approach to patients with psoriasis, they should also be encouraged to correct their modifiable metabolic and cardiovascular risk factors, in particular obesity, sedentariness, alcohol consumption, and smoking habits. This conduct would not only impact the skin disease, but also the overall patient s wellbeing. Taking into account that NAFLD is the major cause of liver enzyme elevation in the western world and that its prevalence is increasing, more research is needed to understand how to successfully manage psoriasis in patients with NAFLD. References 1. Christophers, E. Psoriasis epidemiology and clinical spectrum. Clin Exp Dermatol 2001;26: Schön MP, Boehncke, WH. Psoriasis. N Engl J Med 2005;352: Naldi L, Gambini D. The clinical spectrum of psoriasis. Clinics in Dermatol 2007;25: Lowes MA, Bowcock AM, Krueger JG. Pathogenesis and therapy of psoriasis. Nature 2007;445:
5 5. Koo J, Lee E, Lee CS, Lebwohl M. Psoriasis. J Am Acad Dermatol 2004;50:4 6. Davidovici BB, Sattar N, Prinz JC, Jörg PC, Puig L, Emery P, et al. Psoriasis and systemic inflammatory diseases: potential mechanistic links between skin disease and co-morbid conditions. J Invest Dermatol 2010;130: Gisondi P, Girolomoni G. Cardiometabolic comorbidities and the approach to patients with psoriasis. Actas Dermosifiliogr 2009;100 (Suppl 2): Griffiths CEM. The immunological basis of psoriasis. J Eur Acad Dermatol Venereol 2003;17: Rivera R, Vanaclocha F. Nonalcoholic fatty liver disease and psoriasis. Actas Dermosifiliogr 2010;101: Farley E, Menter A. Psoriasis: comorbidities and associations. G Ital Dermatol Venereol 2011;146: Gisondi P, Targher G, Zoppini G, Girolomoni G. Non-alcoholic fatty liver disease in patients with chronic plaques psoriasis. J Hepatol 2009;51: Farrel GC, Larter CZ. Non-alcoholic fatty liver disease: From steatosis to cirrhosis. Hepatol 2006;43: S99-S Paschos P, Paleta K. Non alcoholic fatty liver disease and metabolic syndrome. Hippokratia 2009;13: Gisondi P, Ferrazzi A, Girolomoni G. Metabolic comorbidities and psoriasis. Acta Dermatovenerol Croat 2010;18: Karnikowiski M, Córdova C, Oliveira RJ, Karnikowski MGO, Nóbrega OT,. Non-alcoholic fatty liver disease and metabolic syndrome in Brazilian median-aged and older adults. Sao Paulo Med J 2007;125: Adams LA, Angulo P. Recent concepts in non-alcoholic fatty liver disease. Diabet Med 2005;22: Bitencourt AGV, Cotrim HP, Alves E, Almeida AM, Barbosa DBV, Santos AS et al. Doença hepática gordurosa não alcoólica: características clínicas e histológicas em obesos graves submetidos a cirurgia bariátrica. Acta Gastroenterol Latinoam 2007;37: Anstee QM, Daly AK, Day CP. Genetics of alcoholic and nonalcoholic fatty liver disease. Semin Liver Dis 2011;31: Lonardo A, Loria P, Leonardi F, Borsatti A, Neri P, Pulvirenti M, et al. Fasting insulin and uric acid levels but not indices of iron metabolism are independent predictors of non-alcoholic fatty liver disease. A case-control study. Digestive and Liver Diseases 2002;34: Madanagobalane S, Anandan S. The increased prevalence of non-alcoholic fatty liver disease in psoriatic patients: a study from South India. Australas J Dermatol 2012;53: Wenk KS, Arrington KC, Erlich A. Psoriasis and nonalcoholic fatty liver disease, J Eur Acad Dermatol Venereol 2011;25: Campanati A, Ganzetti G, Sario AD, Damiani A, Sandroni L, Rosa L, et al. The effect of etanercept on hepatic fibrosis risk in patients with non-alcoholic fatty liver disease, metabolic syndrome, and psoriasis. J Gastroenterol 2012 Oct 13, E-pub before print. 23. Miele L, Vallone S, Cefalo C. Prevalence, characteristics, and severity of non-alcoholic fatty liver disease in patients with chronic plaque psoriasis. J Hepatol 2009;51: Onumah N, Kircik LH. Psoriasis and its comorbidities. J Drugs Dermatol 2012;11: Menter A, Griffiths CE, Tebbey PW, Horn EJ, Sterry W. Exploring the association between cardiovascular and other disease-related risk factors in the psoriasis population: the need for increased understanding across the medical community. J Eur Acad Dermatol Venereol 2010;24:
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