REVIEW PAPER
Environmental risk factors and epigenetic alternations in psoriasis
 
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1
Dermatology Department of Centre of Postgraduate Medical Education, Warsaw, Poland
 
2
Center of Reproductive Health, Institute of Mother and Child, Warsaw, Poland Department of Obstetrics and Gynecology CSKMSWiA, Warsaw, Poland
 
 
Corresponding author
Marek Roszkiewicz   

Dermatology Department of Centre of Postgraduate Medical Education
 
 
Ann Agric Environ Med. 2020;27(3):335-342
 
KEYWORDS
TOPICS
ABSTRACT
Introduction and objective:
Psoriasis isa quite common, chronic and immune-mediated skin disorder. The prevalence of psoriasis differs in various countries, but it is said to affect 2% of the world’s population in general. Psoriasis has many different clinical features but all lesions have the same characteristic: erythema, thickening and scale, although other clinical features are also connected, such as psoriatic arthritis, obesity and metabolic syndrome. All of these may lead to conditions impairing the quality of life. This review is an attempt to summarize recent data regarding environmental factors, together with epigenetic markers and processes playing an important role in psoriasis.

State of knowledge:
Many different environmental factors play a role in genetically predisposed patients. This is causes epigenetic alternations which may be a linking part in the whole process. Many studies have indicated a connection between psoriasis and various genes and antigens. The presence of HLA-Cw6 is common as well a strong link between its presence and the onset of psoriasis being observed. The main alternations are DNA methylation, histone’s modifications and the role of microRNA. Excessive reaction is usually not present without a triggering factor. Environmental factors are mostly rated, such as drugs, life style and habits (smoking, alcohol), diet, physical trauma (skin injury provoking Koebner phenomenon), stress, microorganism and infections.

Conclusions:
The correlation between pathogenesis of psoriasis and environmental risk factors, together with epigenetic alternations still require more investigation. Education about diet habits, nutrition, weight loss and healthy lifestyle seems to be important during the treatment of psoriasis.

 
REFERENCES (120)
1.
van de Kerkhof PCM, Nestle FO. Psoriasis. In: Bolognia J, Schaffer JV, Cerroni L, editors. Dermatology. Fourth Edition, Elsevier 2017; p. 135–156.
 
2.
Nestle FO, Kaplan DH, Barker J. Psoriasis. N Engl J Med. 2009 Jul 30; 361(5): 496–509.
 
3.
Galezowski A, Maccari F, Hadj-Rabia S, Sigal ML, Phan A, Lahfa M Psoriatic arthritis in France, from infants to the elderly: Findings from two cross-sectional, multicenter studies. Ann Dermatol Venereol. 2017 Nov 13. pii: S0151-9638(17)30968-7.
 
4.
El-Boghdady NA, Ismail MF, Abd-Alhameed MF, Ahmed AS, Ahmed HH Bidirectional Association Between Psoriasis and Obesity: Benefits and Risks. J Interferon Cytokine Res. 2017 Dec 18.
 
5.
Ansarimoghaddam A, Adineh HA, Zareban I, Iranpour S, HosseinZadeh A, Kh F. Prevalence of metabolic syndrome in Middle-East countries: Meta-analysis of cross-sectional studies. Diabetes Metab Syndr. 2017 Dec 2. pii: S1871-4021(17)30350-8.
 
6.
Lebwohl MG, Bachelez H, Barker J, Girolomoni G, Kavanaugh A, Langley RG, et al. Patient perspectives in the management of psoriasis: results from the population-based Multinational Assessment of Psoriasis and Psoriatic Arthritis Survey. J Am Acad Dermatol. 2014 May; 70(5): 871–81.e1–30.
 
7.
Tillett W, Charlton R, Nightingale A, Snowball J, Green A, Smith C, et al. Interval between onset of psoriasis and psoriatic arthritis comparing the UK Clinical Practice Research Datalink with a hospital-based cohort. Rheumatology (Oxford). 2017 Dec 1; 56(12): 2109–2113.
 
8.
Russell TJ, Schultes LM, Kuban DJ. Histocompatibility (HL-A) antigens associated with psoriasis. N Engl J Med. 1972 Oct 12; 287(15): 738–40.
 
9.
Singh S, Pradhan D, Puri P, Ramesh V, Aggarwal S, Nayek A, et al. Genomic alterations driving psoriasis pathogenesis. Gene. 2019 Jan 30; 683: 61–71. doi: 10.1016/j.gene.2018.09.042. Epub 2018 Oct 1.
 
10.
Zeng J, Luo S, Huang Y, Lu Q. Critical role of environmental factors in the pathogenesis of psoriasis. J Dermatol. 2017 Aug; 44(8): 863–872. doi: 10.1111/1346-8138.13806. Epub 2017 Mar 27.
 
11.
Schmitt-Egenolf M, Eiermann TH, Boehncke WH, Ständer M, Sterry W. Familial juvenile onset psoriasis is associated with the human leukocyte antigen (HLA) class I side of the extended haplotype Cw6-B57-DRB1*0701-DQA1*0201-DQB1*0303: a population- and family-based study. J Invest Dermatol. 1996 Apr; 106(4): 711–4.
 
12.
Chen L, Tsai TF. HLA-Cw6 and psoriasis. Br J Dermatol. 2017 Oct 26.
 
13.
Sönmez HE, Batu ED, Demir S, Bilginer Y, Özen S. Comparison of patients with familial Mediterranean fever accompanied with sacroiliitis and patients with juvenile spondyloarthropathy. Clin Exp Rheumatol. 2017 Nov-Dec; 35 Suppl 108(6): 124–127.
 
14.
Dashti N, Javadi Z, Safari F, Farahvash S, Zarebavani M. Estimation of Diagnostic Markers in Rheumatoid Arthritis and Ankylosing Spondylitis. Clin Lab. 2017 Apr 1; 63(4): 797–800.
 
15.
Pasić A, Lipozencić J, Ceović R, Kostović K. The genetics of psoriasis-selected novelties in 2008. Acta Dermatovenerol Croat. 2009; 17(3): 176–81.
 
16.
Tsoi LC, Spain SL, Knight J, Ellinghaus E, Stuart PE, Capon Fm et al. Identification of 15 new psoriasis susceptibility loci highlights the role of innate immunity. Nat Genet. 2012 Dec; 44(12): 1341–8. doi: 10.1038/ng.2467. Epub 2012 Nov 11.
 
17.
Strange A, Capon F, Spencer CC, Knight J, Weale ME, Allen MH et al. A genome-wide association study identifies new psoriasis susceptibility loci and an interaction between HLA-C and ERAP1. Nat Genet. 2010 Nov; 42(11): 985–90. doi: 10.1038/ng.694. Epub 2010 Oct 17.
 
18.
Capon F, Di Meglio P, Szaub J, Prescott NJ, Dunster C, Baumber L, et al. Sequence variants in the genes for the interleukin-23 receptor (IL23R) and its ligand (IL12B) confer protection against psoriasis. Hum Genet. 2007 Sep; 122(2): 201–6. Epub 2007 Jun 22.
 
19.
Di Cesare A, Di Meglio P, Nestle FO. The IL-23/Th17 axis in the immunopathogenesis of psoriasis. J Invest Dermatol. 2009 Jun; 129(6): 1339–50.
 
20.
Trowbridge RM, Pittelkow MR. Epigenetics in the pathogenesis and pathophysiology of psoriasis vulgaris J Drugs Dermatol. 2014 Feb; 13(2): 111–8.
 
21.
Zhao M1, Lu Q. The Aberrant Epigenetic Modifications in the Pathogenesis of Psoriasis. J Investig Dermatol Symp Proc. 2018 Dec; 19(2): S81–S82. doi: 10.1016/j.jisp.2018.09.007.
 
22.
Li Y, Sawalha AH, Lu Q. Aberrant DNA methylation in skin diseases. J Dermatol Sci. 2009 Jun; 54(3): 143–9. doi: 10.1016/j.jdermsci.2009.01.009. Epub 2009 Apr 22.
 
23.
Chen M, Chen ZQ, Cui PG, Yao X, Li YM, Li AS, et al. The methylation pattern of p16INK4a gene promoter in psoriatic epidermis and its clinical significance. Br J Dermatol. 2008 May; 158(5): 987–93. doi: 10.1111/j.1365-2133.2008.08505.x. Epub 2008 Mar 28.
 
24.
Serrano M, Hannon GJ, Beach D. A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature. 1993 Dec 16; 366(6456): 704–7.
 
25.
Brown VL, Harwood CA, Crook T, Cronin JG, Kelsell DP, Proby CM. p16INK4a and p14ARF tumor suppressor genes are commonly inactivated in cutaneous squamous cell carcinoma. J Invest Dermatol. 2004 May; 122(5): 1284–92.
 
26.
Zhang P, Zhao M, Liang G, Yin G, Huang D, Su F, et al. Whole-genome DNA methylation in skin lesions from patients with psoriasis vulgaris. J Autoimmun. 2013 Mar; 41: 17–24. doi: 10.1016/j.jaut.2013.01.001. Epub 2013 Jan 29.
 
27.
Spinola M, Meyer P, Kammerer S, Falvella FS, Boettger MB, Hoyal CR, et al. Association of the PDCD5 locus with lung cancer risk and prognosis in smokers. J Clin Oncol. 2006 Apr 10; 24(11): 1672–8. Epub 2006 Mar 20.
 
28.
Su DM, Zhang Q, Wang X, He P, Zhu YJ, Zhao J, et al. Two types of human malignant melanoma cell lines revealed by expression patterns of mitochondrial and survival-apoptosis genes: implications for malignant melanoma therapy. Mol Cancer Ther. 2009 May; 8(5): 1292–304. doi: 10.1158/1535-7163.MCT-08-1030. Epub 2009 Apr 21.
 
29.
Chandra A, Senapati S, Roy S, Chatterjee G, Chatterjee. Epigenome-wide DNA methylation regulates cardinal pathological features of psoriasis. Clin Epigenetics. 2018 Aug 9; 10(1): 108. doi: 10.1186/s13148-018-0541-9.
 
30.
Ruchusatsawat K, Wongpiyabovorn J, Shuangshoti S, Hirankarn N, Mutirangura A. SHP-1 promoter 2 methylation in normal epithelial tissues and demethylation in psoriasis. J Mol Med (Berl). 2006 Feb; 84(2): 175–82. Epub 2005 Dec 31.
 
31.
Gervin K, Vigeland MD, Mattingsdal M, Hammerø M, Nygård H, Olsen AO, et al. DNA methylation and gene expression changes in monozygotic twins discordant for psoriasis: identification of epigenetically dysregulated genes. PLoS Genet. 2012 Jan; 8(1): e1002454. doi: 10.1371/journal.pgen.1002454. Epub 2012 Jan 19.
 
32.
Nair RP, Duffin KC, Helms C, Ding J, Stuart PE, Goldgar D, et al. Genome-wide scan reveals association of psoriasis with IL-23 and NF-kappaB pathways. Nat Genet. 2009 Feb; 41(2): 199–204. doi: 10.1038/ng.311. Epub 2009 Jan 25.
 
33.
Dixon RA, Diehl RE, Opas E, Rands E, Vickers PJ, Evans JF, et al. Requirement of a 5-lipoxygenase-activating protein for leukotriene synthesis. Nature. 1990 Jan 18; 343(6255): 282–4.
 
34.
Taylor JM, Street TL, Hao L, Copley R, Taylor MS, Hayden PJ, et al. Dynamic and physical clustering of gene expression during epidermal barrier formation in differentiating keratinocytes. PLoS One. 2009 Oct 30; 4(10): e7651. doi: 10.1371/journal.pone.0007651.
 
35.
Holick MF, Chimeh FN, Ray S. Topical PTH (1–34) is a novel, safe and effective treatment for psoriasis: a randomized self-controlled trial and an open trial. Br J Dermatol. 2003 Aug; 149(2): 370–6.
 
36.
Ovejero-Benito MC, Reolid A, Sánchez-Jiménez P, Saiz-Rodríguez M, Muñoz-Aceituno E, Llamas-Velasco M, et al. Histone modifications associated with biological drug response in moderate-to-severepsoriasis. Exp Dermatol. 2018 Dec; 27(12): 1361–1371. doi: 10.1111/exd.13790.
 
37.
Yan JJ, Qiao M, Li RH, Zhao XT, Wang XY, Sun Q. Downregulation of miR-145–5p contributes to hyperproliferation of keratinocytes and skin inflammation in psoriasis. Br J Dermatol. 2018 Sep 30. doi: 10.1111/bjd.17256. [Epub ahead of print].
 
38.
Timis TL, Orasan RI. Understanding psoriasis: Role of miRNAs. Biomed Rep. 2018 Nov; 9(5): 367–374. doi: 10.3892/br.2018.1146. Epub 2018 Sep 11.
 
39.
Wcisło-Dziadecka D, Simka K, Kaźmierczak A, Kruszniewska-Rajs C, Gola J, Grabarek B, et al. Psoriasis Treatment Changes the Expression Profile of Selected Caspases and their Regulatory MicroRNAs. Cell Physiol Biochem. 2018; 50(2): 525–537. doi: 10.1159/000494166. Epub 2018 Oct 11.
 
40.
Wu R, Zeng J, Yuan J, Deng X, Huang Y, Chen L, et al. MicroRNA-210 overexpression promotes psoriasis-like inflammation by inducing Th1 and Th17 cell differentiation. J Clin Invest. 2018 Jun 1; 128(6): 2551–2568. doi: 10.1172/JCI97426. Epub 2018 May 14.
 
41.
Diani M, Altomare G, Reali E. T Helper Cell Subsets in Clinical Manifestations of Psoriasis. J Immunol Res. 2016; 2016: 7692024. doi: 10.1155/2016/7692024. Epub 2016 Aug 10.
 
42.
Krützfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, Manoharan M, et al. Silencing of microRNAs in vivo with ‘antagomirs’. Nature. 2005 Dec 1; 438(7068): 685–9. Epub 2005 Oct 30.
 
43.
Furuhashi T, Saito C, Torii K, Nishida E, Yamazaki S, Morita A. Photo(chemo)therapy reduces circulating Th17 cells and restores circulating regulatory T cells in psoriasis. PLoS One. 2013; 8(1): e54895.
 
44.
Di Meglio P, Nestle FO. The role of IL-23 in the immunopathogenesis of psoriasis. F1000 Biol Rep. 2010 May 24; 2. pii: 40.
 
45.
Girolomoni G, Strohal R, Puig L, Bachelez H, Barker J, Boehncke WH, et al. The role of IL-23 and the IL-23/TH 17 immune axis in the pathogenesis and treatment of psoriasis. J Eur Acad Dermatol Venereol. 2017 Oct; 31(10): 1616–1626.
 
46.
Couderc E, Morel F, Levillain P, Buffière-Morgado A1, Camus M1, Paquier C, et al. Interleukin-17A-induced production of acute serum amyloid A by keratinocytes contributes to psoriasis pathogenesis. PLoS One. 2017 Jul 14; 12(7): e0181486.
 
47.
Naldi L, Chatenoud L, Linder D, Belloni Fortina A, Peserico A, Virgili AR, et al. Cigarette smoking, body mass index, and stressful life events as risk factors for psoriasis: results from an Italian case-control study. J Invest Dermatol. 2005 Jul; 125(1): 61–7.
 
48.
Rachakonda TD, Dhillon JS, Florek AG, Armstrong AW. Effect of tonsillectomy on psoriasis: a systematic review. J Am Acad Dermatol. 2015 Feb; 72(2): 261–75.
 
49.
Gomes-Neto JC, Kittana H, Mantz S, Segura Munoz RR, Schmaltz RJ, Bindels LB, et al. A gut pathobiont synergizes with the microbiota to instigate inflammatory disease marked by immunoreactivity against other symbionts but not itself. Sci Rep. 2017 Dec 18; 7(1): 17707.
 
50.
Wang Y, Gao X, Ghozlane A, Hu H, Li X, Xiao Y, et al. Characteristics of Fecal Microbiota in Pediatric Crohn’s Disease and Their Dynamic Changes During Infliximab Therapy. J Crohns Colitis. 2017 Nov 29.
 
51.
Rasmussen HE, Hamaker BR. Prebiotics and Inflammatory Bowel Disease. Gastroenterol Clin North Am. 2017 Dec; 46(4): 783–795.
 
52.
Halling ML, Kjeldsen J, Knudsen T, Nielsen J, Hansen LK. Patients with inflammatory bowel disease have increased risk of autoimmune and inflammatory diseases. World J Gastroenterol. 2017 Sep 7; 23(33): 6137–6146.
 
53.
Prescott SL, Larcombe DL, Logan AC, West C, Burks W, Caraballo L, et al. The skin microbiome: impact of modern environments on skin ecology, barrier integrity, and systemic immune programming. World Allergy Organ J. 2017 Aug 22; 10(1): 29.
 
54.
Manasson J, Shen N, Garcia Ferrer HR, Ubeda C, Iraheta I, Heguy A et al. Gut Microbiota Perturbations in Reactive Arthritis and Post-Infectious Spondyloarthritis. Arthritis Rheumatol. 2017 Oct 26.
 
55.
Shir A, Klein S, Sagiv-Barfi I, Geiger T, Zigler M, Langut Y, et al. S101, an inhibitor of proliferating T-cells, rescues mice from superantigen-induced shock. J Infect Dis. 2017 Nov 15.
 
56.
Ottman N, Smidt H, de Vos WM, Belzer C. The function of our microbiota: who is out there and what do they do? Front Cell Infect Microbiol. 2012 Aug 9; 2: 104.
 
57.
Capurso G, Lahner E. The interaction between smoking, alcohol and the gut microbiome. Best Pract Res Clin Gastroenterol. 2017 Oct; 31(5): 579–588.
 
58.
Landers TF, Cohen B, Wittum TE, Larson EL. A Review of Antibiotic Use in Food Animals: Perspective, Policy, and Potential Public Health Rep. 2012 Jan-Feb; 127(1): 4–22.
 
59.
Nakatsuji T, Chiang HI, Jiang SB, Nagarajan H, Zengler K, Gallo RL. The microbiome extends to subepidermal compartments of normal skin. Nat Commun. 2013; 4: 1431.
 
60.
Zanvit P, Konkel JE, Jiao X, Kasagi S, Zhang D, Wu R, et al. Antibiotics in neonatal life increase murine susceptibility to experimental psoriasis. Nat Commun. 2015 Sep 29; 6: 8424.
 
61.
Rosenbaum JT, Asquith MJ. The Microbiome: a Revolution in Treatment for Rheumatic Diseases? Curr Rheumatol Rep. 2016 Oct; 18(10): 62.
 
62.
Breban M. Gut microbiota and inflammatory joint diseases. Joint Bone Spine. 2016 Dec; 83(6): 645–649.
 
63.
Scarpa R, Manguso F, D’Arienzo A, D’Armiento FP, Astarita C, Mazzacca G, et al. Microscopic inflammatory changes in colon of patients with both active psoriasis and psoriatic arthritis without bowel symptoms. J Rheumatol. 2000 May; 27(5): 1241–6.
 
64.
Telesford KM, Yan W, Ochoa-Reparaz J, Pant A, Kircher C, Christy MA, et al. A commensal symbiotic factor derived from Bacteroides fragilis promotes human CD39(+)Foxp3(+) T cells and Treg function. Gut Microbes. 2015 Jul 4; 6(4): 234–42.
 
65.
Thorleifsdottir RH, Sigurdardottir SL, Sigurgeirsson B, Olafsson JH, Petersen H, Sigurdsson MI, et al. HLA-Cw6 homozygosity in plaque psoriasis is associated with streptococcal throat infections and pronounced improvement after tonsillectomy: A prospective case series. J Am Acad Dermatol. 2016 Nov; 75(5): 889–896.
 
66.
Ruiz-Romeu E, Ferran M, Sagristà M, Olafsson JH, Petersen H, Sigurdsson MI, et al. Streptococcus pyogenes-induced cutaneous lymphocyte antigen-positive T cell-dependent epidermal cell activation triggers TH17 responses in patients with guttate psoriasis. J Allergy Clin Immunol. 2016 Aug; 138(2): 491–499.e6.
 
67.
Yan D, Issa N, Afifi L, Jeon C, Chang HW, Liao W. The Role of the Skin and Gut Microbiome in Psoriatic Disease. Curr Dermatol Rep. 2017 Jun; 6(2): 94–103.
 
68.
Arck P, Handjiski B, Hagen E, Pincus M, Bruenahl C, Bienenstock J, et al. Is there a ‚gut-brain-skin axis‘? Exp Dermatol. 2010 May; 19(5): 401–5.
 
69.
Varghese R, Rajappa M, Chandrashekar L, Kattimani S, Archana M, Munisamy M, et al. Association among stress, hypocortisolism, systemic inflammation, and disease severity in chronic urticaria. Ann Allergy Asthma Immunol. 2016 Apr; 116(4): 344–348.e1.
 
70.
Lin TK, Zhong L, Santiago JL. Association between Stress and the HPA Axis in the Atopic Dermatitis. Int J Mol Sci. 2017 Oct 12; 18(10). pii: E2131.
 
71.
Vegas O, Poligone B, Blackcloud P, Gilmore ES, VanBuskirk J, Ritchlin CT, et al. Chronic social stress Ameliorates psoriasiform dermatitis through upregulation of the Hypothalamic-Pituitary-Adrenal axis. Brain Behav Immun. 2017 Nov 7. pii: S0889-1591(17)30479-8.
 
72.
Zhang H, Caudle Y, Wheeler C, Zhou Y, Stuart C, Yao B, et al. TGF-β1/Smad2/3/Foxp3 signaling is required for chronic stress-induced immune suppression. J Neuroimmunol. 2017 Nov 8. pii: S0165–5728(17): 30465–4.
 
73.
Kang Y, Cai Y, Pan W. Change in gut microbiota for eczema: Implications for novel therapeutic strategies. Allergol Immunopathol (Madr). 2017 Dec 23. pii: S0301–0546(17): 30104–0.
 
74.
Carrascosa JM, Vilavella M, Garcia-Doval I, Carretero G, Vanaclocha F, Daudén E, et al. Body mass index in patients with moderate-to-severe psoriasis in Spain and its impact as an independent risk factor for therapy withdrawal: results of the Biobadaderm Registry. J Eur Acad Dermatol Venereol. 2014 Jul; 28(7): 907–14.
 
75.
Barrea L, Nappi F, Di Somma C, Savanelli MC, Falco A, Balato A, et al. Environmental Risk Factors in Psoriasis: The Point of View of the Nutritionist. Int J Environ Res Public Health. 2016 Jul 22; 13(5).
 
76.
Armstrong AW, Harskamp CT, Armstrong EJ. The association between psoriasis and obesity: a systematic review and metaanalysis of observational studies. Nutr Diabetes. 2012 Dec 3; 2: e54.
 
77.
Fleming P, Kraft J, Gulliver WP, Lynde C. The relationship of obesity with the severity of psoriasis: A systematic review. J. Cutan. Med. Surg. 2015; 19: 450–456.
 
78.
Naldi L, Conti A, Cazzaniga S, Patrizi A, Pazzaglia M, Lanzoni A, et al. Diet and physical exercise in psoriasis: a randomized controlled trial. Br J Dermatol. 2014 Mar; 170(3): 634–42.
 
79.
Voiculescu VM, Lupu M, Papagheorghe L, Giurcaneanu C, Micu E. Psoriasis and metabolic syndrome—Scientific evidence and therapeutic implications. J Med Life 2014; 7: 468–471.
 
80.
Correia B, Torres T. Obesity: a key component of psoriasis. Acta Biomed. 2015 Sep 14; 86(2): 121–9.
 
81.
Carrascosa JM, Rocamora V, Fernandez-Torres RM, Jimenez-Puya R, Moreno JC, Coll-Puigserver N, et al. Obesity and psoriasis: Inflammatory nature of obesity, relationship between psoriasis and obesity, and therapeutic implications. Actas Dermosifiliogr. 2014 Jan-Feb; 105(1): 31–44.
 
82.
Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ, et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest. 2003; 112: 1821–30.
 
83.
La Cava A, Alviggi C, Matarese G. Unraveling the multiple roles of leptin in inflammation and autoimmunity. J Mol Med. 2004; 82: 4–11.
 
84.
Conde, J, Scotece M, Gomez R, López V, Gómez-Reino JJ, Lago F, et al. Adipokines: biofactors from white adipose tissue. A complex hub among inflammation, metabolism, and immunity. Biofactors. 2011 Nov-Dec; 37(6): 413–20.
 
85.
Zhu KJ, Zhang C, Li M, Zhu CY, Shi G, Fan YM. Leptin levels in patients with psoriasis: A meta-analysis. Clin Exp Dermatol. 2013; 38: 478–483.
 
86.
Chen YJ, Wu CY, Shen JL, Chu SY, Chen CK, Chang YT, et al. Psoriasis independently associated with hyper leptinemia contributing to metabolic syndrome. Arch Dermatol. 2008; 144(12): 1571–5.
 
87.
Peluso I, Palmery M. The relationship between body weight and inflammation: Lesson from anti-TNF- antibody therapy. Hum Immunol. 2016 Jan; 77(1): 47–53.
 
88.
Hamminga EA, van der Lely AJ, Neumann HA, Thio HB. Chronic inflammation in psoriasis and obesity: implications for therapy. Med Hypotheses. 2006; 67(4): 768–73.
 
89.
Al-Mutairi N, Nour T. The effect of weight reduction on treatment outcomes in obese patients with psoriasis on biologic therapy: A randomized controlled prospective trial. Expert Opin Biol Ther. 2014 Jun; 14(6): 749–56.
 
90.
Debbaneh M, Millsop JW, Bhatia BK, Koo J, Liao W. Diet and Psoriasis: Part I. Impact of Weight Loss Interventions. J Am Acad Dermatol. 2014 Jul; 71(1): 133–40.
 
91.
Guida, B, Napoleone, A, Trio R, Nastasi A, Balato N, Laccetti R, et al. Energy-restricted, n-3 polyunsaturated fatty acids-rich diet improves the clinical response to immuno-modulating drugs in obese patients with plaque-type psoriasis: A randomized control clinical trial. Clin Nutr. 2014 Jun; 33(3): 399–405.
 
92.
Millsop JW, Bhatia BK, Debbaneh M, Koo J, Liao W. Diet and Psoriasis: Part 3. Role of Nutritional Supplements. J Am Acad Dermatol. 2014 Sep; 71(3): 561–9.
 
93.
Bhatia, Bhavnit K. Koo J, Linos E, Liao W. Diet and Psoriasis: Part 2. Celiac Disease and Role of a Gluten-Free Diet. J Am Acad Dermatol. 2014 Aug; 71(2): 350–8.
 
94.
Murzaku EC, Bronsnick T, Rao B.K. Diet in dermatology: Part II. Melanoma, chronic urticaria, and psoriasis. J Am Acad Dermatol. 2014; 71: 1053.e1–1053.e16.
 
95.
Salas-Salvadó J, Guasch-Ferré M, Lee CH, Estruch R, Clish CB, Ros E. Protective effects of the mediterranean diet on type 2 diabetes and metabolic syndrome. J Nutr. 2016; 146: S920–S927.
 
96.
Esposito K, Giugliano D. Mediterranean diet for primary prevention of cardiovascular disease. N Engl J Med. 2013; 369: 674–675.
 
97.
Esposito K, Di Palo C, Maiorino MI, Petrizzo M, Bellastella G, Siniscalchi I, et al. Long-term effect of mediterranean-style diet and calorie restriction on biomarkers of longevity and oxidative stress in overweight men. Cardiol Res Pract. 2010 Dec 20; 2011: 293916.
 
98.
Armstrong AW, Harskamp CT, Dhillon JS, Armstrong EJ. Psoriasis and smoking: a systematic review and meta-analysis. Br J Dermatol. 2014 Feb; 170(2): 304–14.
 
99.
Zhu KJ, He SM, Sun LD, Hu D, Cheng H, Zhang Z, et al. Smoking and psoriasis: a meta-analysis of case–control studies. J Dermatol Sci. 2011 Aug; 63(2): 126–8.
 
100.
Yanbaeva DG, Dentener MA, Creutzberg EC, Wesseling G, Wouters EF. Systemic effects of smoking.Chest. 2007 May; 131(5): 1557–66.
 
101.
Armstrong AW, Armstrong EJ, Fuller EN, Sockolov ME, Voyles SV. Smoking and pathogenesis of psoriasis: a review of oxidative, inflammatory and genetic mechanisms. Br J Dermatol. 2011; 165: 1162–8.
 
102.
Emre S, Metin A, Demirseren DD, Kilic S, Isikoglu S, Erel O. The relationship between oxidative stress, smoking and the clinical severity of psoriasis. J Eur Acad Dermatol Venereol. 2012; 27: e370–5.
 
103.
Hojgaard P, Glintborg B, Hetland ML, Hansen TH, Lage-Hansen PR, Petersen MH, et al. Association between tobacco smoking and response to tumour necrosis factor alphainhibitor treatment in psoriatic arthritis: results from the DANBIO registry. Ann Rheum Dis. 2015; 74: 2130–2136.
 
104.
Farkas A, Kemeny L. Alcohol, liver, systemic inflammation and skin: a focus on patients with psoriasis. Skin Pharmacol Physiol. 2013; 26(3): 119–26.
 
105.
Weatherhead SC, Farr PM, Reynolds NJ. Spectral effects of UV on psoriasis. Photochem Photobiol Sci. 2013; 12: 47–53.
 
106.
Wolf P, Weger W, Patra V, et al. Desired response to phototherapy versus photo-aggravation in psoriasis: what makes the difference? Exp Dermatol. 2016; 25: 937–944.
 
107.
De Gruijl FR. For better or for worse, UV in psoriasis. Exp Dermatol. 2016; 25: 945–946.
 
108.
Rutter KJ, Watson RE, Cotterell LF, et al. Severely photosensitive psoriasis: a phenotypically defined patient subset. J Invest Dermatol. 2009 Dec; 129(12): 2861–7.
 
109.
Ros AM, Eklund G. Photosensitive psoriasis. An epidemiologic study. J Am Acad Dermatol. 1987 Nov; 17(5 Pt 1): 752–8.
 
110.
Balak DM1, Hajdarbegovic E Drug-induced psoriasis: clinical perspectives. Psoriasis (Auckl). 2017 Dec 7; 7: 87–94. doi: 10.2147/PTT.S126727. eCollection 2017.
 
111.
Kim GK, Del RJ. Drug-provoked psoriasis: is it drug induced or drug aggravated? understanding pathophysiology and clinical relevance. J Clin Aesthet Dermatol. 2010; 3: 32–38.
 
112.
Abel EA, DiCicco LM, Orenberg EK, Fraki JE, Farber EM. Drugs in exacerbation of psoriasis. J Am Acad Dermatol. 1986; 15(5 pt 1).
 
113.
Mrowietz U, Domm S. Systemic steroids in the treatment of psoriasis: what is fact, what is fiction? J Eur Acad Dermatol Venereol. 2013; 27(8): 1022–1025.
 
114.
Ishii-Osai Y, Yoneta A, Mizugaki N, Takahashi H, Yamashita T, et al. Infliximab treatmentinduced paradoxical psoriasiform reaction in patient with psoriasis vulgaris showing positive lymphocyte transportation test reaction. JAAD Case Rep. 2015 Jul 1; 1(4): 230–3.
 
115.
Biljan D, Laufer D, Filaković P, Situm M, Brataljenović T. Psoriasis, mental disorders and stress. Coll Antropol. 2009; 33: 889–92.
 
116.
Baker BS, Powles A, Fry L. Peptidoglycan: a major aetiological factor for psoriasis? Trends Immunol. 2006; 27: 545–551.
 
117.
Park BS, Youn JI. Factors influencing psoriasis: an analysis based upon the extent of involvement and clinical type. J Dermatol. 1998; 25: 97–102.
 
118.
Brufau RM, Brufau RS, Gorgojo MA, et al. Psoriasis lesions are associated with specific types of emotions. Emotional profile in psoriasis. Eur J Dermatol. 2015 Jul-Aug; 25(4): 329–34.
 
119.
Brufau RM, Berna JC, Redondo CB, et al. Personality styles in patients with psoriasis. Anales de Psicologia, 2010; 26: 335–340.
 
120.
Palijan TZ, Kovacević D, Koić E, et al. The impact of psoriasis on the quality of life and psychological characteristics of persons suffering from psoriasis. Coll Antropol. 2011 Sep; 35 Suppl 2: 81–5.
 
eISSN:1898-2263
ISSN:1232-1966
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