Psoriasis and cardiovascular disease: epidemiology, mechanisms, and clinical implications

References

• Langley RG, Krueger GG, Griffiths CE. Psoriasis: epidemiology, clinical features, and quality of life. Ann Rheum Dis. 2005;64 Suppl 2: ii18-ii23; discussion ii24-ii15.
   Google Scholar
• Neimann AL, Shin DB, Wang X, Margolis DJ, Troxel AB, Gelfand JM. Prevalence of cardiovascular risk factors in patients with psoriasis. J Am Acad Dermatol. 2006;55(5):829–835.
   PubMed Web of Science ®Google Scholar
• Al-Mutairi N, Al-Farag S, Al-Mutairi A, Al-Shiltawy M. Comorbidities associated with psoriasis: an experience from the Middle East. J Dermatol. 2010;37(2):146–155.
   PubMed Web of Science ®Google Scholar
• Altobelli E, Petrocelli R, Maccarone M, et al. Risk factors of hypertension, diabetes and obesity in Italian psoriasis patients: a survey on sociodemographic characteristics, smoking habits and alcohol consumption. Eur J Dermatol. 2009;19(3):252–256.
   Web of Science ®Google Scholar
• 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 Derm Venereol 2010;90(2):147–151.
   PubMed Web of Science ®Google Scholar
• Wu Y, Mills D, Bala M. Psoriasis: cardiovascular risk factors and other disease comorbidities. J Drugs Dermatol. 2008;7(4):373–377.
   PubMed Web of Science ®Google Scholar
• Kimball AB, Guerin A, Latremouille-Viau D, et al. Coronary heart disease and stroke risk in patients with psoriasis: retrospective analysis. Am J Med. 2010;123(4):350–357.
   PubMed Web of Science ®Google Scholar
• Lin HW, Wang KH, Lin HC. Increased risk of acute myocardial infarction in patients with psoriasis: a 5-year population-based study in Taiwan. J Am Acad Dermatol. 2011;64(3):495–501.
   Web of Science ®Google Scholar
• Ahlehoff O, Gislason GH, Charlot M, et al. Psoriasis is associated with clinically significant cardiovascular risk: a Danish nationwide cohort study. J Intern Med. 2011;270(2):147–157.
   PubMed Web of Science ®Google Scholar
• Kaye JA, Li L, Jick SS. Incidence of risk factors for myocardial infarction and other vascular diseases in patients with psoriasis. Br J Dermatol. 2008;159(4):895–902.
   PubMed Web of Science ®Google Scholar
• Gelfand JM, Dommasch ED, Shin DB, et al. The risk of stroke in patients with psoriasis. J Invest Dermatol. 2009;129(10):2411–2418.
   PubMed Web of Science ®Google Scholar
• Mehta NN, Yu Y, Pinnelas R, et al. Attributable risk estimate of severe psoriasis on major cardiovascular events. Am J Med. 2011;124(8):775. e771-e776.
   PubMed Web of Science ®Google Scholar
• Mehta NN, Azfar RS, Shin DB, Neimann AL, Troxel AB, Gelfand JM. Patients with severe psoriasis are at increased risk of cardiovascular mortality: cohort study using the General Practice Research Database. Eur Heart J. 2010;31(8):1000–1006.
   PubMed Web of Science ®Google Scholar
• Gelfand JM, Neimann AL, Shin DB, Wang X, Margolis DJ, Troxel AB. Risk of myocardial infarction in patients with psoriasis. JAMA. 2006;296(14):1735–1741.
   PubMed Web of Science ®Google Scholar
• Armstrong AW, Voyles SV, Armstrong EJ, Fuller EN, Rutledge JC. A tale of two plaques: convergent mechanisms of T-cell-mediated inflammation in psoriasis and atherosclerosis. Exp Dermatol. 2011;20(7):544–549.
   PubMed Web of Science ®Google Scholar
• Armstrong AW, Voyles SV, Armstrong EJ, Fuller EN, Rutledge JC. Angiogenesis and oxidative stress: common mechanisms linking psoriasis with atherosclerosis. J Dermatol Sci. 2011;63(1):1–9.
   PubMed Web of Science ®Google Scholar
• Solomon DH, Massarotti E, Garg R, Liu J, Canning C, Schneeweiss S. Association between disease-modifying antirheumatic drugs and diabetes risk in patients with rheumatoid arthritis and psoriasis. JAMA. 2011;305(24):2525–2531.
   PubMed Web of Science ®Google Scholar
• Greenberg JD, Kremer JM, Curtis JR, et al. Tumour necrosis factor antagonist use and associated risk reduction of cardiovascular events among patients with rheumatoid arthritis. Annals of the Rheumatic Diseases. 2011;70(4):576–582.
   PubMed Web of Science ®Google Scholar
• Wu JJ. Abstract: The effect of tumor necrosis factor-alpha inhibitors on the risk of myocardial infarction in patients with psoriasis. Conference: American Academy of Dermatology. 2011.
   Google Scholar
• Abuabara K, Lee H, Kimball AB. The effect of systemic psoriasis therapies on the incidence of myocardial infarction: a cohort study. Br J Dermatol. 2011.
   Web of Science ®Google Scholar
• Kannel WB. Metabolic risk factors for coronary heart disease in women: perspective from the Framingham Study. Am Heart J. 1987;114(2):413–419.
   PubMed Web of Science ®Google Scholar
• Qureshi AA, Choi HK, Setty AR, Curhan GC. Psoriasis and the risk of diabetes and hypertension: a prospective study of US female nurses. Arch Dermatol. 2009;145(4):379–382.
   PubMedGoogle Scholar
• Tsai TF, Wang TS, Hung ST, et al. Epidemiology and comorbidities of psoriasis patients in a national database in Taiwan. J Dermatol Sci. 2011;63(1):40–46.
   PubMed Web of Science ®Google Scholar
• Solomon DH, Love TJ, Canning C, Schneeweiss S. Risk of diabetes among patients with rheumatoid arthritis, psoriatic arthritis and psoriasis. Ann Rheum Dis. 2010;69(12):2114–2117.
   PubMed Web of Science ®Google Scholar
• Mallbris L, Akre O, Granath F, et al. Increased risk for cardiovascular mortality in psoriasis inpatients but not in outpatients. Eur J Epidemiol. 2004;19(3):225–230.
   PubMed Web of Science ®Google Scholar
• Abuabara K, Azfar RS, Shin DB, Neimann AL, Troxel AB, Gelfand JM. Cause-specific mortality in patients with severe psoriasis: a population-based cohort study in the UK. Br J Dermatol. 2010;163(3):586–592.
   PubMed Web of Science ®Google Scholar
• Brauchli YB, Jick SS, Miret M, Meier CR. Psoriasis and risk of incident myocardial infarction, stroke or transient ischaemic attack: an inception cohort study with a nested case-control analysis. Br J Dermatol. 2009;160(5):1048–1056.
   PubMed Web of Science ®Google Scholar
• Stern RS, Huibregtse A. Very severe psoriasis is associated with increased noncardiovascular mortality but not with increased cardiovascular risk. J Invest Dermatol. 2011;131(5):1159–1166.
   PubMed Web of Science ®Google Scholar
• Wakkee M, Thio HB, Prens EP, Sijbrands EJ, Neumann HA. Unfavorable cardiovascular risk profiles in untreated and treated psoriasis patients. Atherosclerosis. 2007;190(1):1–9.
   PubMed Web of Science ®Google Scholar
• Wakkee M, Herings RM, Nijsten T. Psoriasis may not be an independent risk factor for acute ischemic heart disease hospitalizations: results of a large population-based Dutch cohort. J Invest Dermatol. 2010;130(4):962–967.
   PubMed Web of Science ®Google Scholar
• Gelfand JM, Troxel AB, Lewis JD, et al. The risk of mortality in patients with psoriasis: results from a population-based study. Arch Dermatol. 2007;143(12):1493–1499.
   PubMed Web of Science ®Google Scholar
• USPSTF A-Z Topic Guide: US Preventive Services Task Force; 2011.
   Google Scholar
• Friedewald VE, Cather JC, Gelfand JM, et al. AJC editor’s consensus: psoriasis and coronary artery disease. Am J Cardiol. 2008;102(12):1631–1643.
   PubMed Web of Science ®Google Scholar
• Kimball AB, Gladman D, Gelfand JM, et al. National Psoriasis Foundation clinical consensus on psoriasis comorbidities and recommendations for screening. J Am Acad Dermatol. 2008;58(6):1031–1042.
   PubMed Web of Science ®Google Scholar
• Pearson TA, Blair SN, Daniels SR, et al. AHA guidelines for primary prevention of cardiovascular disease and stroke: 2002 update: consensus panel guide to comprehensive risk reduction for adult patients without coronary or other atherosclerotic vascular diseases. American Heart Association Science Advisory and Coordinating Committee. Circulation. 2002;106(3):388–391.
   PubMed Web of Science ®Google Scholar
• Grundy SM, Cleeman JI, Merz CN, et al. Implications of recent clinical trials for the National Cholesterol Education Program Adult Treatment Panel III Guidelines. J Am Coll Cardiol. 2004;44(3):720–732.
   PubMedGoogle Scholar
• Parsi KK, Brezinski EA, Lin TC, Li CS, Armstrong AW. Are patients with psoriasis being screened for cardiovascular risk factors? A study of screening practices and awareness among primary care physicians and cardiologists. J Am Acad Dermatol. 2011.
   Web of Science ®Google Scholar
• Zhang K, Li X, Yin G, Liu Y, Tang X. Functional characterization of T cells differentiated in vitro from bone marrow-derived CD34 cells of psoriatic patients with family history. Exp Dermatol. 2010;19(8):e128–e135.
   Web of Science ®Google Scholar
• Nestle FO, Kaplan DH, Barker J. Psoriasis. N Engl J Med. 2009;361(5):496–509.
   PubMed Web of Science ®Google Scholar
• Robert C, Kupper TS. Inflammatory skin diseases, T cells, and immune surveillance. N Engl J Med. 1999;341(24):1817–1828.
   Web of Science ®Google Scholar
• Rizova H, Nicolas JF, Morel P, et al. The effect of anti-CD4 monoclonal antibody treatment on immunopathological changes in psoriatic skin. J Dermatol Sci. 1994;7(1):1–13.
   Google Scholar
• Libby P. The molecular mechanisms of the thrombotic complications of atherosclerosis. J Intern Med. 2008;263(5):517–527.
   Web of Science ®Google Scholar
• Uyemura K, Demer LL, Castle SC, et al. Cross-regulatory roles of interleukin (IL)-12 and IL-10 in atherosclerosis. J Clin Invest. 1996;97(9):2130–2138.
   PubMed Web of Science ®Google Scholar
• Methe H, Brunner S, Wiegand D, Nabauer M, Koglin J, Edelman ER. Enhanced T-helper-1 lymphocyte activation patterns in acute coronary syndromes. J Am Coll Cardiol. 2005;45(12):1939–1945.
   PubMed Web of Science ®Google Scholar
• Tonel G, Conrad C. Interplay between keratinocytes and immune cells – recent insights into psoriasis pathogenesis. Int J Biochem Cell Biol. 2009;41(5):963–968.
   Web of Science ®Google Scholar
• Numasaki M, Lotze MT, Sasaki H. Interleukin-17 augments tumor necrosis factor-alpha-induced elaboration of proangiogenic factors from fibroblasts. Immunol Lett. 2004;93(1):39–43.
   PubMed Web of Science ®Google Scholar
• Takahashi H, Tsuji H, Hashimoto Y, Ishida-Yamamoto A, Iizuka H. Serum cytokines and growth factor levels in Japanese patients with psoriasis. Clin Exp Dermatol. 2010;35(6):645–649.
   PubMed Web of Science ®Google Scholar
• Zaba LC, Cardinale I, Gilleaudeau P, et al. Amelioration of epidermal hyperplasia by TNF inhibition is associated with reduced Th17 responses. J Exp Med. 2007;204(13):3183–3194.
   PubMed Web of Science ®Google Scholar
• Biasucci LM, Liuzzo G, Grillo RL, et al. Elevated levels of C-reactive protein at discharge in patients with unstable angina predict recurrent instability. Circulation. 1999;99(7):855–860.
   PubMed Web of Science ®Google Scholar
• Hashmi S, Zeng QT. Role of interleukin-17 and interleukin-17-induced cytokines interleukin-6 and interleukin-8 in unstable coronary artery disease. Coron Artery Dis. 2006;17(8):699–706.
   PubMed Web of Science ®Google Scholar
• Chabaud M, Miossec P. The combination of tumor necrosis factor alpha blockade with interleukin-1 and interleukin-17 blockade is more effective for controlling synovial inflammation and bone resorption in an ex vivo model. Arthritis Rheum. 2001;44(6):1293–1303.
   PubMedGoogle Scholar
• George J. Mechanisms of disease: the evolving role of regulatory T cells in atherosclerosis. Nat Clin Pract Cardiovasc Med. 2008;5(9):531–540.
   PubMedGoogle Scholar
• Gotsman I, Gupta R, Lichtman AH. The influence of the regulatory T lymphocytes on atherosclerosis. Arterioscler Thromb Vasc Biol. 2007;27(12):2493–2495.
   Web of Science ®Google Scholar
• Sakaguchi S, Yamaguchi T, Nomura T, Ono M. Regulatory T cells and immune tolerance. Cell. 2008;133(5):775–787.
   PubMed Web of Science ®Google Scholar
• Kagen MH, McCormick TS, Cooper KD. Regulatory T cells in psoriasis. Ernst Schering Res Found Workshop. 2006;56:193–209.
   Google Scholar
• Flisiak I, Chodynicka B, Porebski P, Flisiak R. Association between psoriasis severity and transforming growth factor beta(1) and beta(2) in plasma and scales from psoriatic lesions. Cytokine. 2002;19(3):121–125.
   Web of Science ®Google Scholar
• Flisiak I, Zaniewski P, Chodynicka B. Plasma TGF-beta1, TIMP-1, MMP-1 and IL-18 as a combined biomarker of psoriasis activity. Biomarkers. 2008;13(5):549–556.
   Web of Science ®Google Scholar
• Leivo T, Leivo I, Kariniemi AL, Ke ski-Oja J, Virtanen I. Down -regulation of transforming growth factor-beta receptors I and II is seen in lesional but not non-lesional psoriatic epidermis. Br J Dermatol. 1998;138(1):57–62.
   Web of Science ®Google Scholar
• Mallat Z, Besnard S, Duriez M, et al. Protective role of interleukin-10 in atherosclerosis. Circ Res. 1999;85(8):e17–e24.
   Web of Science ®Google Scholar
• Mallat Z, Gojova A, Marchiol-Fournigault C, et al. Inhibition of transforming growth factor-beta signaling accelerates atherosclerosis and induces an unstable plaque phenotype in mice. Circ Res. 2001;89(10):930–934.
   PubMed Web of Science ®Google Scholar
• De Angelis R, Bugatti L, Del Medico P, Nicolini M, Filosa G. Video-capillaroscopic findings in the microcirculation of the psoriatic plaque. Dermatology. 2002;204(3):236–239.
   Web of Science ®Google Scholar
• Elias PM, Arbiser J, Brown BE, et al. Epidermal vascular endothelial growth factor production is required for permeability barrier homeostasis, dermal angiogenesis, and the development of epidermal hyperplasia: implications for the pathogenesis of psoriasis. Am J Pathol. 2008;173(3):689–699.
   PubMed Web of Science ®Google Scholar
• Heidenreich R, Rocken M, Ghoreschi K. Angiogenesis drives psoriasis pathogenesis. Int J Exp Pathol. 2009;90(3):232–248.
   PubMed Web of Science ®Google Scholar
• Tuschil A, Lam C, Haslberger A, Lindley I. Interleukin-8 stimulates calcium transients and promotes epidermal cell proliferation. J Invest Dermatol. 1992;99(3):294–298.
   Web of Science ®Google Scholar
• Bhushan M, McLaughlin B, Weiss JB, Griffiths CE. Levels of endothelial cell stimulating angiogenesis factor and vascular endothelial growth factor are elevated in psoriasis. Br J Dermatol. 1999;141(6):1054–1060.
   PubMed Web of Science ®Google Scholar
• Markham T, Mullan R, Golden-Mason L, et al. Resolution of endothelial activation and down-regulation of Tie2 receptor in psoriatic skin after infliximab therapy. J Am Acad Dermatol. 2006;54(6):1003–1012.
   PubMed Web of Science ®Google Scholar
• Nofal A, Al-Makhzangy I, Attwa E, Nassar A, Abdalmoati A. Vascular endothelial growth factor in psoriasis: an indicator of disease severity and control. J Eur Acad Dermatol Venereol. 2009;23(7):803–806.
   PubMed Web of Science ®Google Scholar
• Celletti FL, Waugh JM, Amabile PG, Brendolan A, Hilfiker PR, Dake MD. Vascular endothelial growth factor enhances atherosclerotic plaque progression. Nat Med. 2001;7(4):425–429.
   PubMed Web of Science ®Google Scholar
• Bochkov VN, Philippova M, Oskolkova O, et al. Oxidized phospholipids stimulate angiogenesis via autocrine mechanisms, implicating a novel role for lipid oxidation in the evolution of atherosclerotic lesions. Circ Res. 2006;99(8):900–908.
   Web of Science ®Google Scholar
• Stannard AK, Khurana R, Evans IM, Sofra V, Holmes DI, Zachary I. Vascular endothelial growth factor synergistically enhances induction of E-selectin by tumor necrosis factor-alpha. Arterioscler Thromb Vasc Biol. 2007;27(3):494–502.
   Web of Science ®Google Scholar
• Heeschen C, Dimmeler S, Hamm CW, Boersma E, Zeiher AM, Simoons ML. Prognostic significance of angiogenic growth factor serum levels in patients with acute coronary syndromes. Circulation. 2003;107(4):524–530.
   Web of Science ®Google Scholar
• Kastrup J, Jorgensen E, Ruck A, et al. Direct intramyocardial plasmid vascular endothelial growth factor-A165 gene therapy in patients with stable severe angina pectoris A randomized double-blind placebo-controlled study: the Euroinject One trial. J Am Coll Cardiol. 2005;45(7):982–988.
   PubMed Web of Science ®Google Scholar
• Wang F, Lee E, Lowes MA, et al. Prominent production of IL-20 by CD68+/CD11c+ myeloid-derived cells in psoriasis: Gene regulation and cellular effects. J Invest Dermatol. 2006;126(7):1590–1599.
   PubMed Web of Science ®Google Scholar
• Kiortsis DN, Mavridis AK, Vasakos S, Nikas SN, Drosos AA. Effects of infliximab treatment on insulin resistance in patients with rheumatoid arthritis and ankylosing spondylitis. Ann Rheum Dis. 2005;64(5):765–766.
   PubMed Web of Science ®Google Scholar
• Gonzalez-Gay MA, De Matias JM, Gonzalez-Juanatey C, et al. Anti-tumor necrosis factor-alpha blockade improves insulin resistance in patients with rheumatoid arthritis. Clin Exp Rheumatol. 2006;24(1):83–86.
   Web of Science ®Google Scholar
• Tam LS, Tomlinson B, Chu TT, Li TK, Li EK. Impact of TNF inhibition on insulin resistance and lipids levels in patients with rheumatoid arthritis. Clin Rheumatol. 2007;26(9):1495–1498.
   Web of Science ®Google Scholar
• Marra M, Campanati A, Testa R, et al. Effect of etanercept on insulin sensitivity in nine patients with psoriasis. Int J Immunopathol Pharmacol. 2007;20(4):731–736.
   PubMed Web of Science ®Google Scholar
• Spanakis E, Sidiropoulos P, Papadakis J, et al. Modest but sustained increase of serum high density lipoprotein cholesterol levels in patients with inflammatory arthritides treated with infliximab. J Rheumatol. 2006;33(12):2440–2446.
   PubMed Web of Science ®Google Scholar
• Vis M, Nurmohamed MT, Wolbink G, et al. Short term effects of infliximab on the lipid profile in patients with rheumatoid arthritis. J Rheumatol. 2005;32(2):252–255.
   Web of Science ®Google Scholar
• Strober B, Teller C, Yamauchi P, et al. Effects of etanercept on C-reactive protein levels in psoriasis and psoriatic arthritis. Br J Dermatol. 2008;159(2):322–330.
   PubMed Web of Science ®Google Scholar
• Dixon WG, Symmons DP. What effects might anti-TNFalpha treatment be expected to have on cardiovascular morbidity and mortality in rheumatoid arthritis? A review of the role of TNFalpha in cardiovascular pathophysiology. Ann Rheum Dis. 2007;66(9):1132–1136.
   Web of Science ®Google Scholar
• Bassuk SS, Rifai N, Ridker PM. High-sensitivity C-reactive protein: clinical importance. Curr Probl Cardiol. 2004;29(8):439–493.
   PubMed Web of Science ®Google Scholar
• Rocha-Pereira P, Santos-Silva A, Rebelo I, Figueiredo A, Quintanilha A, Teixeira F. Dislipidemia and oxidative stress in mild and in severe psoriasis as a risk for cardiovascular disease. Clin Chim Acta. 2001;303(1–2):33–39.
   PubMed Web of Science ®Google Scholar
• Weitz-Schmidt G. Statins as anti-inflammatory agents. Trends Pharmacol Sci. 2002;23(10):482–486.
   PubMed Web of Science ®Google Scholar
• Ghazizadeh R, Tosa M, Ghazizadeh M. Clinical improvement in psoriasis with treatment of associated hyperlipidemia. Am J Med Sci. 2011;341(5):394–398.
   Web of Science ®Google Scholar
• Mausner-Fainberg K, Luboshits G, Mor A, et al. The effect of HMG-CoA reductase inhibitors on naturally occurring CD4+CD25+ T cells. Atherosclerosis. 2008;197(2):829–839.
   PubMed Web of Science ®Google Scholar
• Shirinsky IV, Shirinsky VS. Efficacy of simvastatin in plaque psoriasis: A pilot study. J Am Acad Dermatol. 2007;57(3):529–531.
   Web of Science ®Google Scholar
• Wolkenstein P, Revuz J, Roujeau JC, Bonnelye G, Grob JJ, Bastuji-Garin S. Psoriasis in France and associated risk factors: results of a case-control study based on a large community survey. Dermatology. 2009;218(2):103–109.
   PubMed Web of Science ®Google Scholar
• Naseri M, Hadipour A, Sepaskhah M, Namazi MR. The remarkable beneficial effect of adding oral simvastatin to topical betamethasone for treatment of psoriasis: a double-blind, randomized, placebo-controlled study. Niger J Med. 2010;19(1):58–61.
   Google Scholar
• Prodanovich S, Ma F, Taylor JR, Pezon C, Fasihi T, Kirsner RS. Methotrexate reduces incidence of vascular diseases in veterans with psoriasis or rheumatoid arthritis. J Am Acad Dermatol. 2005;52(2):262–267.
   PubMed Web of Science ®Google Scholar
• Choi HK, Hernan MA, Seeger JD, Robins JM, Wolfe F. Methotrexate and mortality in patients with rheumatoid arthritis: a prospective study. Lancet. 2002;359(9313):1173–1177.
   PubMed Web of Science ®Google Scholar