Cardiovascular Consequences of Autoimmune Rheumatic Diseases

Author(s): Fabiola Atzeni*, Valeria Nucera, Elisabetta Gerratana, Alessia Fiorenza, Luigi Gianturco, Marco Corda, Piercarlo Sarzi-Puttini

Journal Name: Current Vascular Pharmacology

Volume 18 , Issue 6 , 2020

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Graphical Abstract:


The increased risk of cardiovascular disease (CVD) among patients with autoimmune rheumatic diseases such as rheumatoid arthritis, spondyloarthritis and systemic lupus erythematosus has been extensively documented. Sub-clinical atherosclerosis can be assessed using various non-invasive imaging techniques. However, the mechanisms underlying the higher risk of atherosclerotic CVD in patients with autoimmune rheumatic diseases are not fully known, although they seem to include chronic low-grade systemic inflammation leading to prolonged endothelial activation, accompanied by a pro-thrombotic/pro-coagulant and autoantibody state. Furthermore, sub-clinical atherosclerosis is also influenced by other traditional risk factors for CVD. Including the individual components of the metabolic syndrome (MetS: obesity, impaired glucose metabolism, dyslipidemia and high blood pressure), the degree of which is higher in these patients than in controls. The aim of this narrative review is to discuss the CV manifestations and risk factors involved in the increased risk of CVD among patients with autoimmune rheumatic diseases.

Keywords: Cardiovascular involvement, systemic lupus erythematosus, rheumatoid arthritis, spondyloarthritis, CVD, atherosclerosis.

Avina-Zubieta JA, Thomas J, Sadatsafavi M, Lehman AJ, Lacaille D. Risk of incident cardiovascular events in patients with rheumatoid arthritis: A meta-analysis of observational studies. Ann Rheum Dis 2012; 71(9): 1524-9.
[] [PMID: 22425941]
Aviña-Zubieta JA, Choi HK, Sadatsafavi M, Etminan M, Esdaile JM, Lacaille D. Risk of cardiovascular mortality in patients with rheumatoid arthritis: A meta-analysis of observational studies. Arthritis Rheum 2008; 59(12): 1690-7.
[] [PMID: 19035419]
Mathieu S, Pereira B, Soubrier M. Cardiovascular events in ankylosing spondylitis: An updated meta-analysis. Semin Arthritis Rheum 2015; 44(5): 551-5.
[] [PMID: 25455683]
Polachek A, Touma Z, Anderson M, et al. Risk of cardiovascular morbidity in patients with psoriatic arthritis: A Meta-analysis of observational studies. Arthritis Care Res (Hoboken) 2016; 69(1): 67-74.
[] [PMID: 27111228]
Peters MJ, van Halm VP, Voskuyl AE, et al. Does rheumatoid arthritis equal diabetes mellitus as an independent risk factor for cardiovascular disease? A prospective study. Arthritis Rheum 2009; 61(11): 1571-9.
[] [PMID: 19877093]
Lindhardsen J, Ahlehoff O, Gislason GH, et al. The risk of myocardial infarction in rheumatoid arthritis and diabetes mellitus: A Danish nationwide cohort study. Ann Rheum Dis 2011; 70(6): 929-34.
[] [PMID: 21389043]
Kerekes G, Soltész P, Nurmohamed MT, et al. Validated methods for assessment of subclinical atherosclerosis in rheumatology. Nat Rev Rheumatol 2012; 8(4): 224-34.
[] [PMID: 22349611]
Corrales A, González-Juanatey C, Peiró ME, Blanco R, Llorca J, González-Gay MA. Carotid ultrasound is useful for the cardiovascular risk stratification of patients with rheumatoid arthritis: Results of a population-based study. Ann Rheum Dis 2014; 73(4): 722-7.
[] [PMID: 23505241]
Agca R, Heslinga SC, Rollefstad S, et al. EULAR recommendations for cardiovascular disease risk management in patients with rheumatoid arthritis and other forms of inflammatory joint disorders: 2015/2016 update. Ann Rheum Dis 2017; 76(1): 17-28.
[] [PMID: 27697765]
Di Minno MN, Ambrosino P, Lupoli R, et al. Clinical assessment of endothelial function in patients with rheumatoid arthritis: A meta-analysis of literature studies. Eur J Intern Med 2015; 26(10): 835-42.
[] [PMID: 26547241]
Provan S, Angel K, Semb AG, Atar D, Kvien TK. NT-proBNP predicts mortality in patients with rheumatoid arthritis: Results from 10-year follow-up of the EURIDISS study. Ann Rheum Dis 2010; 69(11): 1946-50.
[] [PMID: 20525846]
Avouac J, Meune C, Chenevier-Gobeaux C, et al. Inflammation and disease activity are associated with high circulating cardiac markers in rheumatoid arthritis independently of traditional cardiovascular risk factors. J Rheumatol 2014; 41(2): 248-55.
[] [PMID: 24334650]
Ku IA, Imboden JB, Hsue PY, Ganz P. Rheumatoid arthritis: Model of systemic inflammation driving atherosclerosis. Circ J 2009; 73(6): 977-85.
[] [PMID: 19430165]
Dessein PH, Solomon A, Woodiwiss AJ, Norton GR, Tsang L, Gonzalez-Gay MA. Marked independent relationship between circulating interleukin-6 concentrations and endothelial activation in rheumatoid arthritis. Mediators Inflamm 2013; 2013: 510243.
[] [PMID: 24453423]
Habets KL, Trouw LA, Levarht EW, et al. Anti-citrullinated protein antibodies contribute to platelet activation in rheumatoid arthritis. Arthritis Res Ther 2015; 17: 209.
[] [PMID: 26268317]
Beinsberger J, Heemskerk JW, Cosemans JM. Chronic arthritis and cardiovascular disease: altered blood parameters give rise to a prothrombotic propensity. Semin Arthritis Rheum 2014; 44(3): 345-52.
[] [PMID: 25077842]
Florence JM, Krupa A, Booshehri LM, Allen TC, Kurdowska AK. Metalloproteinase-9 contributes to endothelial dysfunction in atherosclerosis via protease activated receptor-1. PLoS One 2017; 12(2): e0171427.
[] [PMID: 28166283]
Myasoedova E, Crowson CS, Kremers HM, et al. Lipid paradox in rheumatoid arthritis: the impact of serum lipid measures and systemic inflammation on the risk of cardiovascular disease. Ann Rheum Dis 2011; 70(3): 482-7.
[] [PMID: 21216812]
Schimmel EK, Yazici Y. Increased lipid levels but unchanged atherogenic index in rheumatoid arthritis patients treated with biologic disease modifying antirheumatic drugs: Published experience. Clin Exp Rheumatol 2009; 27: 446-51.
[PMID: 19604437]
Danesh J, Kaptoge S, Mann AG, et al. Long-term interleukin-6 levels and subsequent risk of coronary heart disease: two new prospective studies and a systematic review. PLoS Med 2008; 5(4): e78.
[] [PMID: 18399716]
Kaptoge S, Di Angelantonio E, Lowe G, et al. C-reactive protein concentration and risk of coronary heart disease, stroke, and mortality: an individual participant meta-analysis. Lancet 2010; 375(9709): 132-40.
[] [PMID: 20031199]
Danesh J, Lewington S, Thompson SG, et al. Plasma fibrinogen level and the risk of major cardiovascular diseases and nonvascular mortality: an individual participant meta-analysis. JAMA 2005; 294(14): 1799-809.
[PMID: 16219884]
Libby P. Role of inflammation in atherosclerosis associated with rheumatoid arthritis. Am J Med 2008; 121(10 Suppl. 1): 21-31.
[] [PMID: 18926166]
Rho YH, Chung CP, Oeser A, et al. Inflammatory mediators and premature coronary atherosclerosis in rheumatoid arthritis. Arthritis Rheum 2009; 61(11): 1580-5.
[] [PMID: 19877084]
Ridker PM, Buring JE, Shih J, Matias M, Hennekens CH. Prospective study of C-reactive protein and the risk of future cardiovascular events among apparently healthy women. Circulation 1998; 98(8): 731-3.
[] [PMID: 9727541]
Gonzalez-Gay MA, Gonzalez-Juanatey C, Piñeiro A, Garcia-Porrua C, Testa A, Llorca J. High-grade C-reactive protein elevation correlates with accelerated atherogenesis in patients with rheumatoid arthritis. J Rheumatol 2005; 32(7): 1219-23.
[PMID: 15996055]
Qin B, Yang M, Fu H, et al. Body mass index and the risk of rheumatoid arthritis: A systematic review and dose-response meta-analysis. Arthritis Res Ther 2015; 17: 86.
[] [PMID: 25890172]
Crowson CS, Matteson EL, Davis JM III, Gabriel SE. Contribution of obesity to the rise in incidence of rheumatoid arthritis. Arthritis Care Res (Hoboken) 2013; 65(1): 71-7.
[] [PMID: 22514156]
Lu B, Hiraki LT, Sparks JA, et al. Being overweight or obese and risk of developing rheumatoid arthritis among women: a prospective cohort study. Ann Rheum Dis 2014; 73(11): 1914-22.
[] [PMID: 25057178]
Dessein PH, Woodiwiss AJ, Norton GR, Solomon A. Rheumatoid arthritis is associated with reduced adiposity but not with unfavorable major cardiovascular risk factor profiles and enhanced carotid atherosclerosis in black Africans from a developing population: a cross-sectional study. Arthritis Res Ther 2013; 15(4): R96.
[] [PMID: 23968456]
Challal S, Minichiello E, Boissier M-C, Semerano L. Cachexia and adiposity in rheumatoid arthritis. Relevance for disease management and clinical outcomes. Joint Bone Spine 2016; 83(2): 127-33.
[] [PMID: 26184539]
Metsios GS, Stavropoulos-Kalinoglou A, Douglas KMJ, et al. Blockade of tumour necrosis factor-alpha in rheumatoid arthritis: effects on components of rheumatoid cachexia. Rheumatology (Oxford) 2007; 46(12): 1824-7.
[] [PMID: 18032540]
Stavropoulos-Kalinoglou A, Metsios GS, Koutedakis Y, Kitas GD. Obesity in rheumatoid arthritis. Rheumatology (Oxford) 2011; 50(3): 450-62.
[] [PMID: 20959355]
Stavropoulos-Kalinoglou A, Metsios GS, Panoulas VF, et al. Associations of obesity with modifiable risk factors for the development of cardiovascular disease in patients with rheumatoid arthritis. Ann Rheum Dis 2009; 68(2): 242-5.
[] [PMID: 18677010]
Baghdadi LR, Woodman RJ, Shanahan EM, Mangoni AA. The impact of traditional cardiovascular risk factors on cardiovascular outcomes in patients with rheumatoid arthritis: a systematic review and meta-analysis. PLoS One 2015; 10(2): e0117952.
[] [PMID: 25689371]
Wolfe F, Michaud K. Effect of body mass index on mortality and clinical status in rheumatoid arthritis. Arthritis Care Res (Hoboken) 2012; 64(10): 1471-9.
[] [PMID: 22514152]
Dessein PH, Norton GR, Woodiwiss AJ, Tsang L, Solomon A. Age impacts on the independent relationships of leptin with cardiometabolic risk and surrogate markers of enhanced early atherogenesis in black and white patients with rheumatoid arthritis: a cross-sectional study. Rheumatol Int 2014; 34(3): 329-39.
[] [PMID: 24399454]
Choy E, Sattar N. Interpreting lipid levels in the context of high-grade inflammatory states with a focus on rheumatoid arthritis: a challenge to conventional cardiovascular risk actions. Ann Rheum Dis 2009; 68(4): 460-9.
[] [PMID: 19286905]
Singh U, Dasu MR, Yancey PG, Afify A, Devaraj S, Jialal I. Human C-reactive protein promotes oxidized low density lipoprotein uptake and matrix metalloproteinase-9 release in Wistar rats. J Lipid Res 2008; 49(5): 1015-23.
[] [PMID: 18245817]
Wang X, Liao D, Bharadwaj U, et al. C-reactive protein inhibits cholesterol efflux from human macrophage derived foam cells. Arterioscler Thromb Vasc Biol 2008; 28: 519-26.
[]] [PMID: 18096828]
Watanabe J, Charles-Schoeman C, Miao Y, et al. Proteomic profiling following immunoaffinity capture of high-density lipoprotein: association of acute-phase proteins and complement factors with proinflammatory high-density lipoprotein in rheumatoid arthritis. Arthritis Rheum 2012; 64(6): 1828-37.
[] [PMID: 22231638]
Raterman HG, Levels H, Voskuyl AE, Lems WF, Dijkmans BA, Nurmohamed MT. HDL protein composition alters from proatherogenic into less atherogenic and proinflammatory in rheumatoid arthritis patients responding to rituximab. Ann Rheum Dis 2013; 72(4): 560-5.
[] [PMID: 22589377]
Jamnitski A, Levels JH, van den Oever IA, Nurmohamed MT. High-density lipoprotein profiling changes in patients with rheumatoid arthritis treated with tumor necrosis factor inhibitors: A cohort study. J Rheumatol 2013; 40(6): 825-30.
[] [PMID: 23637327]
Giles JT, Allison M, Bingham CO III, Scott WM Jr, Bathon JM. Adiponectin is a mediator of the inverse association of adiposity with radiographic damage in rheumatoid arthritis. Arthritis Rheum 2009; 61(9): 1248-56.
[] [PMID: 19714593]
Dessein PH, Joffe BI, Stanwix AE. Inflammation, insulin resistance, and aberrant lipid metabolism as cardiovascular risk factors in rheumatoid arthritis. J Rheumatol 2003; 30(7): 1403-5.
[PMID: 12858433]
Boyer JF, Gourraud PA, Cantagrel A, Davignon JL, Constantin A. Traditional cardiovascular risk factors in rheumatoid arthritis: a meta-analysis. Joint Bone Spine 2011; 78(2): 179-83.
[] [PMID: 20851020]
Burska AN, Sakthiswary R, Sattar N. Effects of tumour necrosis factor antagonists on insulin sensitivity/resistance in rheumatoid arthritis: a systematic review and meta-analysis. PLoS One 2015; 10(6): e0128889.
[] [PMID: 26110878]
González-Gay MA, González-Juanatey C. Inflammation and lipid profile in rheumatoid arthritis: bridging an apparent paradox. Ann Rheum Dis 2014; 73(7): 1281-3.
[] [PMID: 24907362]
McCarey DW, McInnes IB, Madhok R, et al. Trial of Atorvastatin in rheumatoid arthritis (TARA): double-blind, randomised placebo-controlled trial. Lancet 2004; 363(9426): 2015-21.
[] [PMID: 15207950]
Sheng X, Murphy MJ, Macdonald TM, Wei L. Effectiveness of statins on total cholesterol and cardiovascular disease and all-cause mortality in osteoarthritis and rheumatoid arthritis. J Rheumatol 2012; 39(1): 32-40.
[] [PMID: 22045835]
Kitas GD, Nightingale P, Armitage J, Sattar N, Belch JJF, Symmons DPM. Trial of atorvastatin for the primary prevention of cardiovascular events in patients with rheumatoid arthritis (TRACE RA): A multicenter, randomized, placebo controlled trial. Arthritis Rheumatol 2019; 71(9): 1437-49.
Kremers HM, Crowson CS, Therneau TM, Roger VL, Gabriel SE. High ten-year risk of cardiovascular disease in newly diagnosed rheumatoid arthritis patients: a population-based cohort study. Arthritis Rheum 2008; 58(8): 2268-74.
[] [PMID: 18668561]
Chung CP, Giles JT, Petri M, et al. Prevalence of traditional modifiable cardiovascular risk factors in patients with rheumatoid arthritis: comparison with control subjects from the multi-ethnic study of atherosclerosis. Semin Arthritis Rheum 2012; 41(4): 535-44.
[] [PMID: 22340996]
Dalbeni A, Giollo A, Tagetti A, et al. Traditional cardiovascular risk factors or inflammation: Which factors accelerate atherosclerosis in arthritis patients? Int J Cardiol 2017; 236: 488-92.
[] [PMID: 28109577]
Siebert S, Lyall DM, Mackay DF, et al. Characteristics of rheumatoid arthritis and its association with major comorbid conditions: cross-sectional study of 502 649 UK Biobank participants. RMD Open 2016; 2(1): e000267.
[] [PMID: 27403335]
Panoulas VF, Douglas KM, Milionis HJ, et al. Prevalence and associations of hypertension and its control in patients with rheumatoid arthritis. Rheumatology (Oxford) 2007; 46(9): 1477-82.
[] [PMID: 17704521]
Baka Z, Buzás E, Nagy G. Rheumatoid arthritis and smoking: putting the pieces together. Arthritis Res Ther 2009; 11(4): 238.
[] [PMID: 19678909]
Gonzalez A, Maradit Kremers H, Crowson CS, et al. Do cardiovascular risk factors confer the same risk for cardiovascular outcomes in rheumatoid arthritis patients as in non-rheumatoid arthritis patients? Ann Rheum Dis 2008; 67(1): 64-9.
[] [PMID: 17517756]
Zhang J, Fu L, Shi J, et al. The risk of metabolic syndrome in patients with rheumatoid arthritis: a meta-analysis of observational studies. PLoS One 2013; 8(10): e78151.
[] [PMID: 24205134]
Sattar N, McCarey DW, Capell H, McInnes IB. Explaining how “high-grade” systemic inflammation accelerates vascular risk in rheumatoid arthritis. Circulation 2003; 108(24): 2957-63.
[] [PMID: 14676136]
Khan MA. Update on spondyloarthropathies. Ann Intern Med 2002; 136(12): 896-907.
[] [PMID: 12069564]
Radford EP, Doll R, Smith PG. Mortality among patients with ankylosing spondylitis not given X-ray therapy. N Engl J Med 1977; 297(11): 572-6.
[] [PMID: 887115]
Van Doornum S, McColl G, Wicks IP. Accelerated atherosclerosis: an extraarticular feature of rheumatoid arthritis? Arthritis Rheum 2002; 46(4): 862-73.
[] [PMID: 11953961]
Peters MJ, van der Horst-Bruinsma IE, Dijkmans BA, Nurmohamed MT. Cardiovascular risk profile of patients with spondylarthropathies, particularly ankylosing spondylitis and psoriatic arthritis. Semin Arthritis Rheum 2004; 34(3): 585-92.
[] [PMID: 15609262]
Callahan LF, Pincus T. Mortality in the rheumatic diseases. Arthritis Care Res 1995; 8(4): 229-41.
[] [PMID: 8605261]
Kaprove RE, Little AH, Graham DC, Rosen PS. Ankylosing spondylitis: Survival in men with and without radiotherapy. Arthritis Rheum 1980; 23(1): 57-61.
[] [PMID: 7352944]
Khan MA, Khan MK, Kushner I. Survival among patients with ankylosing spondylitis: a life-table analysis. J Rheumatol 1981; 8(1): 86-90.
[PMID: 7218263]
Lehtinen K. Cause of death in 79 patients with ankylosing spondylitis. Scand J Rheumatol 1980; 9(3): 145-7.
[] [PMID: 7455621]
O’Neill TW, Bresnihan B. The heart in ankylosing spondylitis. Ann Rheum Dis 1992; 51(6): 705-6.
[] [PMID: 1616349]
Youssef W, Russell AS. Cardiac, ocular, and renal manifestations of seronegative spondyloarthropathies. Curr Opin Rheumatol 1990; 2(4): 582-5.
[] [PMID: 2206799]
Nagyhegyi G, Nadas I, Banyai F, et al. Cardiac and cardiopulmonary disorders in patients with ankylosing spondylitis and rheumatoid arthritis. Clin Exp Rheumatol 1988; 6(1): 17-26.
[PMID: 3396245]
Bergfeldt L, Edhag O, Vedin L, Vallin H. Ankylosing spondylitis: an important cause of severe disturbances of the cardiac conduction system. Prevalence among 223 pacemaker-treated men. Am J Med 1982; 73(2): 187-91.
[] [PMID: 7114075]
Ribeiro P, Morley KD, Shapiro LM, Garnett RAF, Hughes GRV, Goodwin JF. Left ventricular function in patients with ankylosing spondylitis and Reiter’s disease. Eur Heart J 1984; 5(5): 419-22.
[] [PMID: 6734652]
Sukenik S, Pras A, Buskila D, Katz A, Snir Y, Horowitz J. Cardiovascular manifestations of ankylosing spondylitis. Clin Rheumatol 1987; 6(4): 588-92.
[] [PMID: 3449309]
Ford ES. Does exercise reduce inflammation? Physical activity and C-reactive protein among U.S. adults. Epidemiology 2002; 13(5): 561-8.
[] [PMID: 12192226]
Bergfeldt L, Möller E. Complete heart block--another HLA B27 associated disease manifestation. Tissue Antigens 1983; 21(5): 385-90.
[] [PMID: 6868058]
Doran MF, Brophy S, MacKay K, Taylor G, Calin A. Predictors of longterm outcome in ankylosing spondylitis. J Rheumatol 2003; 30(2): 316-20.
[PMID: 12563688]
Joven J, Rubiés-Prat J, Ras MR, de la Figuera M, Lience E, Masdeu S. High density lipoprotein cholesterol subfractions and apoprotein A-I in patients with rheumatoid arthritis and ankylosing spondylitis. Arthritis Rheum 1984; 27(10): 1199-200.
[] [PMID: 6435642]
Jones SM, Harris CP, Lloyd J, Stirling CA, Reckless JP, McHugh NJ. Lipoproteins and their subfractions in psoriatic arthritis: Identification of an atherogenic profile with active joint disease. Ann Rheum Dis 2000; 59(11): 904-9.
[] [PMID: 11053070]
Calle EE, Thun MJ, Petrelli JM, Rodriguez C, Heath CW Jr. Body-mass index and mortality in a prospective cohort of U.S. adults. N Engl J Med 1999; 341(15): 1097-105.
[] [PMID: 10511607]
Redelmeier DA, Tan SH, Booth GL. The treatment of unrelated disorders in patients with chronic medical diseases. N Engl J Med 1998; 338(21): 1516-20.
[] [PMID: 9593791]
Mayer EL, Jacobsen DW, Robinson K. Homocysteine and coronary atherosclerosis. J Am Coll Cardiol 1996; 27(3): 517-27.
[] [PMID: 8606260]
Ernst E, Resch KL. Fibrinogen as a cardiovascular risk factor: A meta-analysis and review of the literature. Ann Intern Med 1993; 118(12): 956-63.
[] [PMID: 8489110]
Thaulow E, Erikssen J, Sandvik L, Stormorken H, Cohn PF. Blood platelet count and function are related to total and cardiovascular death in apparently healthy men. Circulation 1991; 84(2): 613-7.
[] [PMID: 1860204]
Prasad A, Zhu J, Halcox JP, Waclawiw MA, Epstein SE, Quyyumi AA. Predisposition to atherosclerosis by infections: role of endothelial dysfunction. Circulation 2002; 106(2): 184-90.
[] [PMID: 12105156]
Helliwell PS, Marchesoni A, Peters M, Platt R, Wright V. Cytidine deaminase activity, C reactive protein, histidine, and erythrocyte sedimentation rate as measures of disease activity in psoriatic arthritis. Ann Rheum Dis 1991; 50(6): 362-5.
[] [PMID: 2059079]
Arida A, Protogerou AD, Konstantonis G, et al. Subclinical atherosclerosis is not accelerated in patients with ankylosing spondylitis with low disease activity: new data and metaanalysis of published studies. J Rheumatol 2015; 42(11): 2098-105.
[] [PMID: 26428207]
Schjerning Olsen AM, Fosbøl EL, Lindhardsen J, et al. Duration of treatment with nonsteroidal anti-inflammatory drugs and impact on risk of death and recurrent myocardial infarction in patients with prior myocardial infarction: a nationwide cohort study. Circulation 2011; 123(20): 2226-35.
[] [PMID: 21555710]
Gladman DD, Farewell VT, Wong K, Husted J. Mortality studies in psoriatic arthritis: results from a single outpatient center. II. Prognostic indicators for death. Arthritis Rheum 1998; 41(6): 1103-10.
[<1103:AID-ART18>3.0.CO;2-N] [PMID: 9627021]
Wong K, Gladman DD, Husted J, Long JA, Farewell VT. Mortality studies in psoriatic arthritis: results from a single outpatient clinic. I. Causes and risk of death. Arthritis Rheum 1997; 40(10): 1868-72.
[] [PMID: 9336423]
Di Minno MN, Ambrosino P, Lupoli R, et al. Cardiovascular risk markers in patients with psoriatic arthritis: A meta-analysis of literature studies. Ann Med 2015; 47(4): 346-53.
[] [PMID: 25953378]
Chambless LE, Heiss G, Folsom AR, et al. Association of coronary heart disease incidence with carotid arterial wall thickness and major risk factors: the atherosclerosis risk in communities (ARIC) study, 1987-1993. Am J Epidemiol 1997; 146(6): 483-94.
[] [PMID: 9290509]
van der Meer IM, Bots ML, Hofman A, del Sol AI, van der Kuip DA, Witteman JC. Predictive value of noninvasive measures of atherosclerosis for incident myocardial infarction: the Rotterdam study. Circulation 2004; 109(9): 1089-94.
[] [PMID: 14993130]
Willerson JT, Ridker PM. Inflammation as a cardiovascular risk factor. Circulation 2004; 109(21 Suppl. 1): II2-II10.
[PMID: 15173056]
Di Minno MN, Iervolino S, Peluso R, Scarpa R, Di Minno G. Platelet reactivity and disease activity in subjects with psoriatic arthritis. J Rheumatol 2012; 39(2): 334-6.
[] [PMID: 22174208]
Shimbo D, Grahame-Clarke C, Miyake Y, et al. The association between endothelial dysfunction and cardiovascular outcomes in a population-based multi-ethnic cohort. Atherosclerosis 2007; 192(1): 197-203.
[] [PMID: 16762358]
Yim KM, Armstrong AW. Updates on cardiovascular comorbidities associated with psoriatic diseases: Epidemiology and mechanisms. Rheumatol Int 2017; 37: 97-105.
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): 829-35.
[] [PMID: 17052489]
Takeshita J, Wang S, Shin DB, et al. Effect of psoriasis severity on hypertension control: a population-based study in the United Kingdom. JAMA Dermatol 2015; 151(2): 161-9.
[] [PMID: 25322196]
Khalid U, Hansen PR, Gislason GH, et al. Psoriasis and new-onset diabetes: a Danish nationwide cohort study. Diabetes Care 2013; 36(8): 2402-7.
[] [PMID: 23491525]
Langan SM, Seminara NM, Shin DB, et al. Prevalence of metabolic syndrome in patients with psoriasis: a population-based study in the United Kingdom. J Invest Dermatol 2012; 132(3 Pt 1): 556-62.
[] [PMID: 22113483]
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): 147-57.
[] [PMID: 21114692]
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): 544-9.
[] [PMID: 21692858]
Boehncke WH, Boehncke S, Tobin AM, Kirby B. The ‘psoriatic march’: A concept of how severe psoriasis may drive cardiovascular comorbidity. Exp Dermatol 2011; 20(4): 303-7.
[] [PMID: 21410760]
Buerger C, Richter B, Woth K, et al. Interleukin-1β interferes with epidermal homeostasis through induction of insulin resistance: Implications for psoriasis pathogenesis. J Invest Dermatol 2012; 132(9): 2206-14.
[] [PMID: 22513786]
Yu Y, Sheth N, Krishnamoorthy P, et al. Aortic vascular inflammation in psoriasis is associated with HDL particle size and concentration: A pilot study. Am J Cardiovasc Dis 2012; 2(4): 285-92.
[PMID: 23173102]
Brezinski EA, Follansbee MR, Armstrong EJ, Armstrong AW. Endothelial dysfunction and the effects of TNF inhibitors on the endothelium in psoriasis and psoriatic arthritis: a systematic review. Curr Pharm Des 2014; 20(4): 513-28.
[] [PMID: 23565632]
Agmon-Levin N, Mosca M, Petri M, Shoenfeld Y. Systemic lupus erythematosus one disease or many? Autoimmun Rev 2012; 11(8): 593-5.
[] [PMID: 22041578]
Urowitz MB, Bookman AA, Koehler BE, Gordon DA, Smythe HA, Ogryzlo MA. The bimodal mortality pattern of systemic lupus erythematosus. Am J Med 1976; 60(2): 221-5.
[] [PMID: 1251849]
Doria A, Iaccarino L, Ghirardello A, et al. Long-term prognosis and causes of death in systemic lupus erythematosus. Am J Med 2006; 119(8): 700-6.
[] [PMID: 16887417]
Schoenfeld SR, Kasturi S, Costenbader KH. The epidemiology of atherosclerotic cardiovascular disease among patients with SLE: a systematic review. Semin Arthritis Rheum 2013; 43(1): 77-95.
[] [PMID: 23422269]
Manzi S, Meilahn EN, Rairie JE, et al. Age-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus: Comparison with the Framingham Study. Am J Epidemiol 1997; 145(5): 408-15.
[] [PMID: 9048514]
Ward MM. Premature morbidity from cardiovascular and cerebrovascular diseases in women with systemic lupus erythematosus. Arthritis Rheum 1999; 42(2): 338-46.
[<338:AID-ANR17>3.0.CO;2-U] [PMID: 10025929]
Bengtsson C, Ohman ML, Nived O, Rantapää Dahlqvist S. Cardiovascular event in systemic lupus erythematosus in northern Sweden: incidence and predictors in a 7-year follow-up study. Lupus 2012; 21(4): 452-9.
[] [PMID: 22065097]
Zöller B, Li X, Sundquist J, Sundquist K. Risk of subsequent ischemic and hemorrhagic stroke in patients hospitalized for immune-mediated diseases: a nationwide follow-up study from Sweden. BMC Neurol 2012; 12: 41.
[] [PMID: 22708578]
Urowitz MB, Gladman D, Ibañez D, et al. Atherosclerotic vascular events in a multinational inception cohort of systemic lupus erythematosus. Arthritis Care Res (Hoboken) 2010; 62(6): 881-7.
[] [PMID: 20535799]
Dhakal BP, Kim CH, Al-Kindi SG, Oliveira GH. Heart failure in systemic lupus erythematosus. Trends Cardiovasc Med 2018; 28(3): 187-97.
[] [PMID: 28927572]
Buss SJ, Wolf D, Korosoglou G, et al. Myocardial left ventricular dysfunction in patients with systemic lupus erythematosus: new insights from tissue Doppler and strain imaging. J Rheumatol 2010; 37(1): 79-86.
[] [PMID: 19955054]
Wislowska M, Dereń D, Kochmański M, Sypuła S, Rozbicka J. Systolic and diastolic heart function in SLE patients. Rheumatol Int 2009; 29(12): 1469-76.
[] [PMID: 19319538]
Mok CC, Ho LY, To CH. Annual incidence and standardized incidence ratio of cerebrovascular accidents in patients with systemic lupus erythematosus. Scand J Rheumatol 2009; 38(5): 362-8.
[] [PMID: 19296403]
Bertoli AM, Vilá LM, Alarcón GS, et al. Factors associated with arterial vascular events in PROFILE: a multiethnic lupus cohort. Lupus 2009; 18(11): 958-65.
[] [PMID: 19762396]
Gustafsson J, Gunnarsson I, Börjesson O, et al. Predictors of the first cardiovascular event in patients with systemic lupus erythematosus - a prospective cohort study. Arthritis Res Ther 2009; 11(6): R186.
[] [PMID: 20003285]
Gustafsson JT, Simard JF, Gunnarsson I, et al. Risk factors for cardiovascular mortality in patients with systemic lupus erythematosus, a prospective cohort study. Arthritis Res Ther 2012; 14(2): R46.
[] [PMID: 22390680]
Giannelou M, Mavragani CP. Cardiovascular disease in systemic lupus erythematosus: A comprehensive update. J Autoimmun 2017; 82: 1-12.
[] [PMID: 28606749]
Parodis I, Sjöwall C, Jönsen A, et al. Smoking and pre-existing organ damage reduce the efficacy of belimumab in systemic lupus erythematosus. Autoimmun Rev 2017; 16(4): 343-51.
[] [PMID: 28216072]
Blum CB, Levy RI. Role of dietary intervention in the primary prevention of coronary heart disease. Individuals with high-normal or elevated serum cholesterol levels should be placed on cholesterol-lowering diets. Cardiology 1987; 74(1): 2-21.
[] [PMID: 3545472]
Olusi SO, George S. Prevalence of LDL atherogenic phenotype in patients with systemic lupus erythematosus. Vasc Health Risk Manag 2011; 7: 75-80.
[] [PMID: 21415920]
Hahn BH, Grossman J, Ansell BJ, Skaggs BJ, McMahon M. Altered lipoprotein metabolism in chronic inflammatory states: proinflammatory high-density lipoprotein and accelerated atherosclerosis in systemic lupus erythematosus and rheumatoid arthritis. Arthritis Res Ther 2008; 10(4): 213.
[] [PMID: 18828865]
Delgado Alves J, Kumar S, Isenberg DA. Cross-reactivity between anti-cardiolipin, anti-high-density lipoprotein and anti-apolipoprotein A-I IgG antibodies in patients with systemic lupus erythematosus and primary antiphospholipid syndrome. Rheumatology (Oxford) 2003; 42(7): 893-9.
[] [PMID: 12730551]
Petri M, Perez-Gutthann S, Spence D, Hochberg MC. Risk factors for coronary artery disease in patients with systemic lupus erythematosus. Am J Med 1992; 93(5): 513-9.
[] [PMID: 1442853]
Sabio JM, Vargas-Hitos JA, Navarrete-Navarrete N, et al. Prevalence of and factors associated with hypertension in young and old women with systemic lupus erythematosus. J Rheumatol 2011; 38(6): 1026-32.
[] [PMID: 21406497]
Kiani AN, Post WS, Magder LS, Petri M. Predictors of progression in atherosclerosis over 2 years in systemic lupus erythematosus. Rheumatology (Oxford) 2011; 50(11): 2071-9.
[] [PMID: 21875880]
Chung CP, Avalos I, Oeser A, et al. High prevalence of the metabolic syndrome in patients with systemic lupus erythematosus: Association with disease characteristics and cardiovascular risk factors. Ann Rheum Dis 2007; 66(2): 208-14.
[] [PMID: 16901956]
Mok CC, Poon WL, Lai JP, et al. Metabolic syndrome, endothelial injury, and subclinical atherosclerosis in patients with systemic lupus erythematosus. Scand J Rheumatol 2010; 39(1): 42-9.
[] [PMID: 20132070]
Parker B, Urowitz MB, Gladman DD, et al. Impact of early disease factors on metabolic syndrome in systemic lupus erythematosus: data from an international inception cohort. Ann Rheum Dis 2015; 74(8): 1530-6.
[] [PMID: 24692585]
Tyrrell PN, Beyene J, Feldman BM, McCrindle BW, Silverman ED, Bradley TJ. Rheumatic disease and carotid intima-media thickness: a systematic review and meta-analysis. Arterioscler Thromb Vasc Biol 2010; 30(5): 1014-26.
[] [PMID: 20150560]
Celermajer DS, Sorensen KE, Gooch VM, et al. Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet 1992; 340(8828): 1111-5.
[] [PMID: 1359209]
Henrot P, Foret J, Barnetche T, et al. Assessment of subclinical atherosclerosis in systemic lupus erythematosus: A systematic review and meta-analysis. Joint Bone Spine 2018; 85(2): 155-63.
[] [PMID: 29288864]
Tziomalos K, Gkougkourelas I, Sarantopoulos A, et al. Arterial stiffness and peripheral arterial disease in patients with systemic lupus erythematosus. Rheumatol Int 2017; 37(2): 293-8.
[] [PMID: 27873008]
McMahon M, Grossman J, Skaggs B, et al. Dysfunctional proinflammatory high-density lipoproteins confer increased risk of atherosclerosis in women with systemic lupus erythematosus. Arthritis Rheum 2009; 60(8): 2428-37.
[] [PMID: 19644959]
Delgado Alves J, Ames PR, Donohue S, et al. Antibodies to high-density lipoprotein and beta2-glycoprotein I are inversely correlated with paraoxonase activity in systemic lupus erythematosus and primary antiphospholipid syndrome. Arthritis Rheum 2002; 46(10): 2686-94.
[] [PMID: 12384928]
Batuca JR, Ames PR, Amaral M, Favas C, Isenberg DA, Delgado Alves J. Anti-atherogenic and anti-inflammatory properties of high-density lipoprotein are affected by specific antibodies in systemic lupus erythematosus. Rheumatology (Oxford) 2009; 48(1): 26-31.
[] [PMID: 19000993]
Avalos I, Chung CP, Oeser A, et al. Oxidative stress in systemic lupus erythematosus: Relationship to disease activity and symptoms. Lupus 2007; 16(3): 195-200.
[] [PMID: 17432105]
Margutti P, Matarrese P, Conti F, et al. Autoantibodies to the C-terminal subunit of RLIP76 induce oxidative stress and endothelial cell apoptosis in immune-mediated vascular diseases and atherosclerosis. Blood 2008; 111(9): 4559-70.
[] [PMID: 17993611]
Dieudé M, Senécal JL, Raymond Y. Induction of endothelial cell apoptosis by heat-shock protein 60-reactive antibodies from anti-endothelial cell autoantibody-positive systemic lupus erythematosus patients. Arthritis Rheum 2004; 50(10): 3221-31.
[] [PMID: 15476243]
Meroni PL, Raschi E, Testoni C, Borghi MO. Endothelial cell activation by antiphospholipid antibodies. Clin Immunol 2004; 112(2): 169-74.
[] [PMID: 15240160]
Somers EC, Zhao W, Lewis EE, et al. Type I interferons are associated with subclinical markers of cardiovascular disease in a cohort of systemic lupus erythematosus patients. PLoS One 2012; 7(5)e37000
[] [PMID: 22606325]
Mozzini C, Garbin U, Fratta Pasini AM, Cominacini L. An exploratory look at NETosis in atherosclerosis. Intern Emerg Med 2017; 12(1): 13-22.
[] [PMID: 27655025]
Rajagopalan S, Somers EC, Brook RD, et al. Endothelial cell apoptosis in systemic lupus erythematosus: A common pathway for abnormal vascular function and thrombosis propensity. Blood 2004; 103(10): 3677-83.
[] [PMID: 14726373]
Zheng SL, Roddick AJ. Association of aspirin use for primary prevention with cardiovascular events and bleeding events: a systematic review and meta-analysis. JAMA 2019; 321(3): 277-87.
[] [PMID: 30667501]
Savarese G, De Ferrari GM, Rosano GM, Perrone-Filardi P. Safety and efficacy of ezetimibe: A meta-analysis. Int J Cardiol 2015; 201: 247-52.
[] [PMID: 26301648]
Gasparyan AY, Stavropoulos-Kalinoglou A, Mikhailidis DP, Douglas KM, Kitas GD. Platelet function in rheumatoid arthritis: Arthritic and cardiovascular implications. Rheumatol Int 2011; 31(2): 153-64.
[] [PMID: 20390282]
Fanouriakis A, Kostopoulou M, Alunno A, et al. 2019 update of the EULAR recommendations for the management of systemic lupus erythematosus. Ann Rheum Dis 2019; 78(6): 736-45.
[] [PMID: 30926722]
Iudici M, Fasano S, Gabriele Falcone L, et al. Low-dose aspirin as primary prophylaxis for cardiovascular events in systemic lupus erythematosus: A long-term retrospective cohort study. Rheumatology (Oxford) 2016; 55(9): 1623-30.
[] [PMID: 27247433]
Xing B, Yin Y-F, Zhao L-D, et al. Effect of 3-hydroxy-3-methylglutaryl-coenzyme a reductase inhibitor on disease activity in patients with rheumatoid arthritis: A meta-analysis. Medicine (Baltimore) 2015; 94(8): e572.
[] [PMID: 25715256]

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Year: 2020
Page: [566 - 579]
Pages: 14
DOI: 10.2174/1570161118666200127142936
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