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Current Vascular Pharmacology

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ISSN (Print): 1570-1611
ISSN (Online): 1875-6212

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Review Article

Cardiovascular Disease in Systemic Lupus Erythematosus: Recent Data on Epidemiology, Risk Factors and Prevention

Author(s): Myrto Kostopoulou , Dionysis Nikolopoulos, Ioannis Parodis and George Bertsias *

Volume 18, Issue 6, 2020

Page: [549 - 565] Pages: 17

DOI: 10.2174/1570161118666191227101636

Price: $65

Abstract

Systemic Lupus Erythematosus (SLE) is associated with increased risk for accelerated atherosclerosis and cardiovascular (CV) events including coronary heart disease, cerebrovascular and peripheral artery disease. CV events occur both early and late during the disease course, with younger patients being at much higher risk than age-matched counterparts. The risk cannot be fully accounted for by the increased prevalence of traditional atherosclerotic factors and may be due to pathophysiologic intermediates such as type I interferons and other inflammatory cytokines, oxidative stress, activated granulocytes and production of extracellular chromatin traps, antiphospholipid and other autoantibodies causing dysfunction of lipoproteins, altogether resulting in endothelial injury and pro-atherogenic dyslipidaemia. These mechanisms may be further aggravated by chronic intake of prednisone (even at doses <7.5 mg/day), whereas immunomodulatory drugs, especially hydroxychloroquine, may exert antiatherogenic properties. To date, there is a paucity of randomized studies regarding the effectiveness of preventative strategies and pharmacological interventions specifically in patients with SLE. Nevertheless, both the European League Against Rheumatism recommendations and extrapolated evidence from the general population emphasize that SLE patients should undergo regular monitoring for atherosclerotic risk factors and calculation of the 10-year CV risk. Risk stratification should include diseaserelated factors and accordingly, general (lifestyle modifications/smoking cessation, antihypertensive and statin treatment, low-dose aspirin in selected cases) and SLE-specific (control of disease activity, minimization of glucocorticoids, use of hydroxychloroquine) preventive measures be applied as appropriate. Further studies will be required regarding the use of non-invasive tools and biomarkers for CV assessment and of risk-lowering strategies tailored to SLE.

Keywords: Autoimmune disease, type I interferon, antiphospholipid antibodies, glucocorticoids, dyslipidaemia, ischemic heart disease, cerebrovascular disease, statin.

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[1]
Tsokos GC. Systemic lupus erythematosus. N Engl J Med 2011; 365(22): 2110-21.
[http://dx.doi.org/10.1056/NEJMra1100359] [PMID: 22129255]
[2]
Rúa-Figueroa I, Fernández Castro M, Andreu JL, et al. Comorbidities in patients with primary Sjögren’s syndrome and systemic lupus erythematosus: a comparative registries-based study. Arthritis Care Res (Hoboken) 2017; 69(1): 38-45.
[http://dx.doi.org/10.1002/acr.23015] [PMID: 27564390]
[3]
Barnado A, Carroll RJ, Casey C, Wheless L, Denny JC, Crofford LJ. Phenome-wide association study identifies marked increased in burden of comorbidities in African Americans with systemic lupus erythematosus. Arthritis Res Ther 2018; 20(1): 69.
[http://dx.doi.org/10.1186/s13075-018-1561-8] [PMID: 29636090]
[4]
Tselios K, Gladman DD, Sheane BJ, Su J, Urowitz M. All-cause, cause-specific and age-specific standardised mortality ratios of patients with systemic lupus erythematosus in Ontario, Canada over 43 years (1971-2013). Ann Rheum Dis 2019; 78(6): 802-6.
[http://dx.doi.org/10.1136/annrheumdis-2018-214802] [PMID: 30992296]
[5]
Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 2005; 352(16): 1685-95.
[http://dx.doi.org/10.1056/NEJMra043430] [PMID: 15843671]
[6]
Ahmadi A, Argulian E, Leipsic J, Newby DE, Narula J. From subclinical atherosclerosis to plaque progression and acute coronary events: JACC state-of-the-art review. J Am Coll Cardiol 2019; 74(12): 1608-17.
[http://dx.doi.org/10.1016/j.jacc.2019.08.012] [PMID: 31537271]
[7]
Kutom AH, Gibbs HR. Myocardial infarction due to intracoronary thrombi without significant coronary artery disease in systemic lupus erythematosus. Chest 1991; 100(2): 571-2.
[http://dx.doi.org/10.1378/chest.100.2.571] [PMID: 1864145]
[8]
Asanuma Y, Oeser A, Shintani AK, et al. Premature coronary-artery atherosclerosis in systemic lupus erythematosus. N Engl J Med 2003; 349(25): 2407-15.
[http://dx.doi.org/10.1056/NEJMoa035611] [PMID: 14681506]
[9]
Roman MJ, Shanker BA, Davis A, et al. Prevalence and correlates of accelerated atherosclerosis in systemic lupus erythematosus. N Engl J Med 2003; 349(25): 2399-406.
[http://dx.doi.org/10.1056/NEJMoa035471] [PMID: 14681505]
[10]
Gustafsson JT, Svenungsson E. Definitions of and contributions to cardiovascular disease in systemic lupus erythematosus. Autoimmunity 2014; 47(2): 67-76.
[http://dx.doi.org/10.3109/08916934.2013.856005] [PMID: 24228980]
[11]
Lane HA, Smith JC, Davies JS. Noninvasive assessment of preclinical atherosclerosis. Vasc Health Risk Manag 2006; 2(1): 19-30.
[http://dx.doi.org/10.2147/vhrm.2006.2.1.19] [PMID: 17319466]
[12]
Soltész P, Kerekes G, Dér H, et al. Comparative assessment of vascular function in autoimmune rheumatic diseases: considerations of prevention and treatment. Autoimmun Rev 2011; 10(7): 416-25.
[http://dx.doi.org/10.1016/j.autrev.2011.01.004] [PMID: 21281743]
[13]
Matsuzawa Y, Kwon TG, Lennon RJ, Lerman LO, Lerman A. Prognostic value of flow-mediated vasodilation in brachial artery and fingertip artery for cardiovascular events: a systematic review and meta-analysis. J Am Heart Assoc 2015; 4(11): e002270.
[http://dx.doi.org/10.1161/JAHA.115.002270] [PMID: 26567372]
[14]
Kim HL, Kim SH. Pulse wave velocity in atherosclerosis. Front Cardiovasc Med 2019; 6: 41.
[http://dx.doi.org/10.3389/fcvm.2019.00041] [PMID: 31024934]
[15]
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.
[http://dx.doi.org/10.1016/0002-9343(76)90431-9] [PMID: 1251849]
[16]
Ståhl-Hallengren C, Jönsen A, Nived O, Sturfelt G. Incidence studies of systemic lupus erythematosus in Southern Sweden: increasing age, decreasing frequency of renal manifestations and good prognosis. J Rheumatol 2000; 27(3): 685-91.
[PMID: 10743809]
[17]
Alamanos Y, Voulgari PV, Papassava M, Tsamandouraki K, Drosos AA. Survival and mortality rates of systemic lupus erythematosus patients in northwest Greece. Study of a 21-year incidence cohort. Rheumatology (Oxford) 2003; 42(9): 1122-3.
[http://dx.doi.org/10.1093/rheumatology/keg291] [PMID: 12923275]
[18]
Mok CC, Tse SM, Chan KL, Ho LY. Effect of the metabolic syndrome on organ damage and mortality in patients with systemic lupus erythematosus: a longitudinal analysis. Clin Exp Rheumatol 2018; 36(3): 389-95.
[PMID: 29148424]
[19]
Tselios K, Gladman DD, Su J, Ace O, Urowitz MB. Evolution of risk factors for atherosclerotic cardiovascular events in systemic lupus erythematosus: a longterm prospective study. J Rheumatol 2017; 44(12): 1841-9.
[http://dx.doi.org/10.3899/jrheum.161121] [PMID: 29093154]
[20]
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.
[http://dx.doi.org/10.1177/0961203309104862] [PMID: 19762396]
[21]
Magder LS, Petri M. Incidence of and risk factors for adverse cardiovascular events among patients with systemic lupus erythematosus. Am J Epidemiol 2012; 176(8): 708-19.
[http://dx.doi.org/10.1093/aje/kws130] [PMID: 23024137]
[22]
Pons-Estel GJ, González LA, Zhang J, et al. Predictors of cardiovascular damage in patients with systemic lupus erythematosus: data from LUMINA (LXVIII), a multiethnic US cohort. Rheumatology (Oxford) 2009; 48(7): 817-22.
[http://dx.doi.org/10.1093/rheumatology/kep102] [PMID: 19454606]
[23]
Ballocca F, D’Ascenzo F, Moretti C, et al. Predictors of cardiovascular events in patients with systemic lupus erythematosus (SLE): a systematic review and meta-analysis. Eur J Prev Cardiol 2015; 22(11): 1435-41.
[http://dx.doi.org/10.1177/2047487314546826] [PMID: 25139772]
[24]
Ward MM. Premature morbidity from cardiovascular and cerebrovascular diseases in women with systemic lupus erythematosus. Arthritis Rheum 1999; 42(2): 338-46.
[http://dx.doi.org/10.1002/1529-0131(199902)42:2<338:AID-ANR17>3.0.CO;2-U] [PMID: 10025929]
[25]
Bartels CM, Buhr KA, Goldberg JW, et al. Mortality and cardiovascular burden of systemic lupus erythematosus in a US population-based cohort. J Rheumatol 2014; 41(4): 680-7.
[http://dx.doi.org/10.3899/jrheum.130874] [PMID: 24532834]
[26]
Hak AE, Karlson EW, Feskanich D, Stampfer MJ, Costenbader KH. Systemic lupus erythematosus and the risk of cardiovascular disease: results from the nurses’ health study. Arthritis Rheum 2009; 61(10): 1396-402.
[http://dx.doi.org/10.1002/art.24537] [PMID: 19790130]
[27]
Esdaile JM, Abrahamowicz M, Grodzicky T, et al. Traditional Framingham risk factors fail to fully account for accelerated atherosclerosis in systemic lupus erythematosus. Arthritis Rheum 2001; 44(10): 2331-7.
[http://dx.doi.org/10.1002/1529-0131(200110)44:10<2331:AID-ART395>3.0.CO;2-I] [PMID: 11665973]
[28]
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.
[http://dx.doi.org/10.1093/oxfordjournals.aje.a009122] [PMID: 9048514]
[29]
Aviña-Zubieta JA, To F, Vostretsova K, De Vera M, Sayre EC, Esdaile JM. Risk of myocardial infarction and stroke in newly diagnosed systemic lupus erythematosus: a general population-based study. Arthritis Care Res (Hoboken) 2017; 69(6): 849-56.
[http://dx.doi.org/10.1002/acr.23018] [PMID: 28129475]
[30]
Tektonidou MG, Kravvariti E, Konstantonis G, Tentolouris N, Sfikakis PP, Protogerou A. subclinical atherosclerosis in systemic lupus erythematosus: comparable risk with diabetes mellitus and rheumatoid arthritis. Autoimmun Rev 2017; 16(3): 308-12.
[http://dx.doi.org/10.1016/j.autrev.2017.01.009] [PMID: 28147263]
[31]
Bulkley BH, Roberts WC. The heart in systemic lupus erythematosus and the changes induced in it by corticosteroid therapy. A study of 36 necropsy patients. Am J Med 1975; 58(2): 243-64.
[http://dx.doi.org/10.1016/0002-9343(75)90575-6] [PMID: 1115070]
[32]
Haider YS, Roberts WC. Coronary arterial disease in systemic lupus erythematosus; quantification of degrees of narrowing in 22 necropsy patients (21 women) aged 16 to 37 years. Am J Med 1981; 70(4): 775-81.
[http://dx.doi.org/10.1016/0002-9343(81)90532-5] [PMID: 7211914]
[33]
de Leeuw K, Smit AJ, de Groot E, van Roon AM, Kallenberg CG, Bijl M. Longitudinal study on premature atherosclerosis in patients with systemic lupus erythematosus. Atherosclerosis 2009; 206(2): 546-50.
[http://dx.doi.org/10.1016/j.atherosclerosis.2009.03.018] [PMID: 19389674]
[34]
Haque S, Skeoch S, Rakieh C, et al. Progression of subclinical and clinical cardiovascular disease in a UK SLE cohort: the role of classic and SLE-related factors. Lupus Sci Med 2018; 5(1): e000267.
[http://dx.doi.org/10.1136/lupus-2018-000267] [PMID: 30538814]
[35]
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.
[http://dx.doi.org/10.1093/rheumatology/ker285] [PMID: 21875880]
[36]
Roman MJ, Crow MK, Lockshin MD, et al. Rate and determinants of progression of atherosclerosis in systemic lupus erythematosus. Arthritis Rheum 2007; 56(10): 3412-9.
[http://dx.doi.org/10.1002/art.22924] [PMID: 17907140]
[37]
Thompson T, Sutton-Tyrrell K, Wildman RP, et al. Progression of carotid intima-media thickness and plaque in women with systemic lupus erythematosus. Arthritis Rheum 2008; 58(3): 835-42.
[http://dx.doi.org/10.1002/art.23196] [PMID: 18311797]
[38]
Svenungsson E, Jensen-Urstad K, Heimbürger M, et al. Risk factors for cardiovascular disease in systemic lupus erythematosus. Circulation 2001; 104(16): 1887-93.
[http://dx.doi.org/10.1161/hc4101.097518] [PMID: 11602489]
[39]
Wu GC, Liu HR, Leng RX, et al. Subclinical atherosclerosis in patients with systemic lupus erythematosus: A systemic review and meta-analysis. Autoimmun Rev 2016; 15(1): 22-37.
[http://dx.doi.org/10.1016/j.autrev.2015.10.002] [PMID: 26455562]
[40]
Kao AH, Lertratanakul A, Elliott JR, et al. Relation of carotid intima-media thickness and plaque with incident cardiovascular events in women with systemic lupus erythematosus. Am J Cardiol 2013; 112(7): 1025-32.
[http://dx.doi.org/10.1016/j.amjcard.2013.05.040] [PMID: 23827400]
[41]
Goldberg RJ, Urowitz MB, Ibañez D, Nikpour M, Gladman DD. Risk factors for development of coronary artery disease in women with systemic lupus erythematosus. J Rheumatol 2009; 36(11): 2454-61.
[http://dx.doi.org/10.3899/jrheum.090011] [PMID: 19833754]
[42]
Telles RW, Lanna CC, Sousa AJ, et al. Progression of carotid atherosclerosis in patients with systemic lupus erythematosus. Clin Rheumatol 2013; 32(9): 1293-300.
[http://dx.doi.org/10.1007/s10067-013-2264-9] [PMID: 23620348]
[43]
Wang P, Mao YM, Zhao CN, et al. Increased pulse wave velocity in systemic lupus erythematosus: a meta-analysis. Angiology 2018; 69(3): 228-35.
[http://dx.doi.org/10.1177/0003319717715964] [PMID: 28635303]
[44]
Fernández-Nebro A, Rúa-Figueroa Í, López-Longo FJ, et al. Cardiovascular events in systemic lupus erythematosus: a nationwide study in Spain from the relesser registry. Medicine (Baltimore) 2015; 94(29): e1183.
[http://dx.doi.org/10.1097/MD.0000000000001183] [PMID: 26200625]
[45]
Eder L, Gladman DD, Ibañez D, Urowitz MB. The correlation between carotid artery atherosclerosis and clinical ischemic heart disease in lupus patients. Lupus 2014; 23(11): 1142-8.
[http://dx.doi.org/10.1177/0961203314537696] [PMID: 24876099]
[46]
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.
[http://dx.doi.org/10.1186/ar3759] [PMID: 22390680]
[47]
Baragetti A, Ramirez GA, Magnoni M, et al. Disease trends over time and CD4+CCR5+ T-cells expansion predict carotid atherosclerosis development in patients with systemic lupus erythematosus. Nutr Metab Cardiovasc Dis 2018; 28(1): 53-63.
[http://dx.doi.org/10.1016/j.numecd.2017.09.001] [PMID: 29150407]
[48]
Karp I, Abrahamowicz M, Fortin PR, et al. Recent corticosteroid use and recent disease activity: independent determinants of coronary heart disease risk factors in systemic lupus erythematosus? Arthritis Rheum 2008; 59(2): 169-75.
[http://dx.doi.org/10.1002/art.23352] [PMID: 18240259]
[49]
Barsalou J, Bradley TJ, Tyrrell PN, et al. Impact of disease duration on vascular surrogates of early atherosclerosis in childhood-onset systemic lupus erythematosus. Arthritis Rheumatol 2016; 68(1): 237-46.
[http://dx.doi.org/10.1002/art.39423] [PMID: 26361097]
[50]
Fasano S, Margiotta DP, Navarini L, et al. Primary prevention of cardiovascular disease in patients with systemic lupus erythematosus: case series and literature review. Lupus 2017; 26(14): 1463-72.
[http://dx.doi.org/10.1177/0961203317722847] [PMID: 28786768]
[51]
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.
[http://dx.doi.org/10.1093/rheumatology/kew231] [PMID: 27247433]
[52]
Rhoads JP, Major AS. How oxidized low-density lipoprotein activates inflammatory responses. Crit Rev Immunol 2018; 38(4): 333-42.
[http://dx.doi.org/10.1615/CritRevImmunol.2018026483] [PMID: 30806246]
[53]
Hallenbeck JM, Hansson GK, Becker KJ. Immunology of ischemic vascular disease: plaque to attack. Trends Immunol 2005; 26(10): 550-6.
[http://dx.doi.org/10.1016/j.it.2005.08.007] [PMID: 16109503]
[54]
Sherer Y, Shoenfeld Y. Mechanisms of disease: atherosclerosis in autoimmune diseases. Nat Clin Pract Rheumatol 2006; 2(2): 99-106.
[http://dx.doi.org/10.1038/ncprheum0092] [PMID: 16932663]
[55]
Denny MF, Thacker S, Mehta H, et al. Interferon-alpha promotes abnormal vasculogenesis in lupus: a potential pathway for premature atherosclerosis. Blood 2007; 110(8): 2907-15.
[http://dx.doi.org/10.1182/blood-2007-05-089086] [PMID: 17638846]
[56]
Thacker SG, Zhao W, Smith CK, et al. Type I interferons modulate vascular function, repair, thrombosis, and plaque progression in murine models of lupus and atherosclerosis. Arthritis Rheum 2012; 64(9): 2975-85.
[http://dx.doi.org/10.1002/art.34504] [PMID: 22549550]
[57]
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.
[http://dx.doi.org/10.1371/journal.pone.0037000] [PMID: 22606325]
[58]
Lee PY, Li Y, Richards HB, et al. Type I interferon as a novel risk factor for endothelial progenitor cell depletion and endothelial dysfunction in systemic lupus erythematosus. Arthritis Rheum 2007; 56(11): 3759-69.
[http://dx.doi.org/10.1002/art.23035] [PMID: 17968925]
[59]
Crow MK. Type I interferon in the pathogenesis of lupus. J Immunol 2014; 192(12): 5459-68.
[http://dx.doi.org/10.4049/jimmunol.1002795] [PMID: 24907379]
[60]
Goossens P, Gijbels MJ, Zernecke A, et al. Myeloid type I interferon signaling promotes atherosclerosis by stimulating macrophage recruitment to lesions. Cell Metab 2010; 12(2): 142-53.
[http://dx.doi.org/10.1016/j.cmet.2010.06.008] [PMID: 20674859]
[61]
Diao Y, Mohandas R, Lee P, et al. Effects of long-term type i interferon on the arterial wall and smooth muscle progenitor cells differentiation. Arterioscler Thromb Vasc Biol 2016; 36(2): 266-73.
[http://dx.doi.org/10.1161/ATVBAHA.115.306767] [PMID: 26634654]
[62]
Tydén H, Lood C, Gullstrand B, et al. Endothelial dysfunction is associated with activation of the type I interferon system and platelets in patients with systemic lupus erythematosus. RMD Open 2017; 3(2): e000508.
[http://dx.doi.org/10.1136/rmdopen-2017-000508] [PMID: 29119007]
[63]
Svenungsson E, Fei GZ, Jensen-Urstad K, de Faire U, Hamsten A, Frostegard J. TNF-alpha: a link between hypertriglyceridaemia and inflammation in SLE patients with cardiovascular disease. Lupus 2003; 12(6): 454-61.
[http://dx.doi.org/10.1191/0961203303lu412oa] [PMID: 12873047]
[64]
Rho YH, Chung CP, Oeser A, et al. Novel cardiovascular risk factors in premature coronary atherosclerosis associated with systemic lupus erythematosus. J Rheumatol 2008; 35(9): 1789-94.
[PMID: 18634156]
[65]
Benagiano M, Borghi MO, Romagnoli J, et al. Interleukin-17/Interleukin-21 and Interferon-g producing T cells specific for beta2 Glycoprotein I in atherosclerosis inflammation of systemic lupus erythematosus patients with antiphospholipid syndrome. Haematologica 2019; 104(12): 2519-27.
[66]
Shovman O, Gilburd B, Shoenfeld Y. The role of inflammatory cytokines in the pathogenesis of systemic lupus erythematosus-related atherosclerosis: a novel target for treatment? J Rheumatol 2006; 33(3): 445-7.
[PMID: 16511912]
[67]
Asanuma Y, Chung CP, Oeser A, et al. Increased concentration of proatherogenic inflammatory cytokines in systemic lupus erythematosus: relationship to cardiovascular risk factors. J Rheumatol 2006; 33(3): 539-45.
[PMID: 16463434]
[68]
Ahmad HM, Sarhan EM, Komber U. Higher circulating levels of OxLDL % of LDL are associated with subclinical atherosclerosis in female patients with systemic lupus erythematosus. Rheumatol Int 2014; 34(5): 617-23.
[http://dx.doi.org/10.1007/s00296-013-2875-0] [PMID: 24101173]
[69]
McMahon M, Grossman J, FitzGerald J, et al. Proinflammatory high-density lipoprotein as a biomarker for atherosclerosis in patients with systemic lupus erythematosus and rheumatoid arthritis. Arthritis Rheum 2006; 54(8): 2541-9.
[http://dx.doi.org/10.1002/art.21976] [PMID: 16868975]
[70]
O’Neill SG, Giles I, Lambrianides A, et al. Antibodies to apolipoprotein A-I, high-density lipoprotein, and C-reactive protein are associated with disease activity in patients with systemic lupus erythematosus. Arthritis Rheum 2010; 62(3): 845-54.
[http://dx.doi.org/10.1002/art.27286] [PMID: 20131231]
[71]
Matsuura E, Kobayashi K, Inoue K, Lopez LR, Shoenfeld Y. Oxidized LDL/beta2-glycoprotein I complexes: new aspects in atherosclerosis. Lupus 2005; 14(9): 736-41.
[http://dx.doi.org/10.1191/0961203305lu2211oa] [PMID: 16218478]
[72]
Rosales C. Neutrophil: a cell with many roles in inflammation or several cell types? Front Physiol 2018; 9: 113.
[http://dx.doi.org/10.3389/fphys.2018.00113] [PMID: 29515456]
[73]
Gaul DS, Stein S, Matter CM. Neutrophils in cardiovascular disease. Eur Heart J 2017; 38(22): 1702-4.
[http://dx.doi.org/10.1093/eurheartj/ehx244] [PMID: 30052884]
[74]
Knight JS, Kaplan MJ. Lupus neutrophils: ‘NET’ gain in understanding lupus pathogenesis. Curr Opin Rheumatol 2012; 24(5): 441-50.
[http://dx.doi.org/10.1097/BOR.0b013e3283546703] [PMID: 22617827]
[75]
Carlucci PM, Purmalek MM, Dey AK, et al. Neutrophil subsets and their gene signature associate with vascular inflammation and coronary atherosclerosis in lupus. JCI Insight 2018; 3(8): 99276.
[http://dx.doi.org/10.1172/jci.insight.99276] [PMID: 29669944]
[76]
Denny MF, Yalavarthi S, Zhao W, et al. A distinct subset of proinflammatory neutrophils isolated from patients with systemic lupus erythematosus induces vascular damage and synthesizes type I IFNs. J Immunol 2010; 184(6): 3284-97.
[http://dx.doi.org/10.4049/jimmunol.0902199] [PMID: 20164424]
[77]
Neubert E, Meyer D, Rocca F, et al. Chromatin swelling drives neutrophil extracellular trap release. Nat Commun 2018; 9(1): 3767.
[http://dx.doi.org/10.1038/s41467-018-06263-5] [PMID: 30218080]
[78]
Garcia-Romo GS, Caielli S, Vega B, et al. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci Transl Med 2011; 3(73): 73ra20.
[http://dx.doi.org/10.1126/scitranslmed.3001201] [PMID: 21389264]
[79]
Pieterse E, Rother N, Garsen M, et al. Neutrophil extracellular traps drive endothelial-to-mesenchymal transition. Arterioscler Thromb Vasc Biol 2017; 37(7): 1371-9.
[http://dx.doi.org/10.1161/ATVBAHA.117.309002] [PMID: 28495931]
[80]
Schreiber K, Sciascia S, de Groot PG, et al. Antiphospholipid syndrome. Nat Rev Dis Primers 2018; 4: 17103.
[http://dx.doi.org/10.1038/nrdp.2017.103] [PMID: 29321641]
[81]
Tektonidou MG, Laskari K, Panagiotakos DB, Moutsopoulos HM. Risk factors for thrombosis and primary thrombosis prevention in patients with systemic lupus erythematosus with or without antiphospholipid antibodies. Arthritis Rheum 2009; 61(1): 29-36.
[http://dx.doi.org/10.1002/art.24232] [PMID: 19116963]
[82]
de Groot PG, Urbanus RT, Derksen RH. Pathophysiology of thrombotic APS: where do we stand? Lupus 2012; 21(7): 704-7.
[http://dx.doi.org/10.1177/0961203312438631] [PMID: 22635207]
[83]
Zhang X, Xie Y, Zhou H, et al. Involvement of TLR4 in oxidized LDL/β2GPI/anti-β2GPI-induced transformation of macrophages to foam cells. J Atheroscler Thromb 2014; 21(11): 1140-51.
[http://dx.doi.org/10.5551/jat.24372] [PMID: 24998486]
[84]
Sun J, Lundström SL, Zhang B, et al. IgM antibodies against phosphorylcholine promote polarization of T regulatory cells from patients with atherosclerotic plaques, systemic lupus erythematosus and healthy donors. Atherosclerosis 2018; 268: 36-48.
[http://dx.doi.org/10.1016/j.atherosclerosis.2017.11.010] [PMID: 29175653]
[85]
Rahman M, Sing S, Golabkesh Z, et al. IgM antibodies against malondialdehyde and phosphorylcholine are together strong protection markers for atherosclerosis in systemic lupus erythematosus: Regulation and underlying mechanisms. Clin Immunol 2016; 166-167: 27-37.
[http://dx.doi.org/10.1016/j.clim.2016.04.007] [PMID: 27102765]
[86]
Bruce IN, Urowitz MB, Gladman DD, Ibañez D, Steiner G. Risk factors for coronary heart disease in women with systemic lupus erythematosus: the Toronto risk factor study. Arthritis Rheum 2003; 48(11): 3159-67.
[http://dx.doi.org/10.1002/art.11296] [PMID: 14613278]
[87]
Tselios K, Sheane BJ, Gladman DD, Urowitz MB. Optimal monitoring for coronary heart disease risk in patients with systemic lupus erythematosus: a systematic review. J Rheumatol 2016; 43(1): 54-65.
[http://dx.doi.org/10.3899/jrheum.150460] [PMID: 26568591]
[88]
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.
[http://dx.doi.org/10.1016/j.semarthrit.2012.12.002] [PMID: 23422269]
[89]
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.
[http://dx.doi.org/10.1186/ar2878] [PMID: 20003285]
[90]
Nikpour M, Urowitz MB, Ibanez D, Harvey PJ, Gladman DD. Importance of cumulative exposure to elevated cholesterol and blood pressure in development of atherosclerotic coronary artery disease in systemic lupus erythematosus: a prospective proof-of-concept cohort study. Arthritis Res Ther 2011; 13(5): R156.
[http://dx.doi.org/10.1186/ar3473] [PMID: 21955652]
[91]
Atukorala I, Weeratunga P, Kalubowila J, et al. Cardiovascular risk in lupus nephritis: Do renal disease-related and other traditional risk factors play a role? Saudi J Kidney Dis Transpl 2015; 26(3): 526-35.
[http://dx.doi.org/10.4103/1319-2442.157357] [PMID: 26022023]
[92]
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.
[http://dx.doi.org/10.1177/0961203311425524] [PMID: 22065097]
[93]
Haque S, Gordon C, Isenberg D, et al. Risk factors for clinical coronary heart disease in systemic lupus erythematosus: the lupus and atherosclerosis evaluation of risk (LASER) study. J Rheumatol 2010; 37(2): 322-9.
[http://dx.doi.org/10.3899/jrheum.090306] [PMID: 19955047]
[94]
Tselios K, Gladman DD, Su J, Urowitz MB. Does renin-angiotensin system blockade protect lupus nephritis patients from atherosclerotic cardiovascular events? A case-control study. Arthritis Care Res (Hoboken) 2016; 68(10): 1497-504.
[http://dx.doi.org/10.1002/acr.22857] [PMID: 26866934]
[95]
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.
[http://dx.doi.org/10.1002/acr.20122] [PMID: 20535799]
[96]
Doria A, Shoenfeld Y, Wu R, et al. Risk factors for subclinical atherosclerosis in a prospective cohort of patients with systemic lupus erythematosus. Ann Rheum Dis 2003; 62(11): 1071-7.
[http://dx.doi.org/10.1136/ard.62.11.1071] [PMID: 14583570]
[97]
Manzi S, Selzer F, Sutton-Tyrrell K, et al. Prevalence and risk factors of carotid plaque in women with systemic lupus erythematosus. Arthritis Rheum 1999; 42(1): 51-60.
[http://dx.doi.org/10.1002/1529-0131(199901)42:1<51:AID-ANR7>3.0.CO;2-D] [PMID: 9920014]
[98]
Schanberg LE, Sandborg C, Barnhart HX, et al. Premature atherosclerosis in pediatric systemic lupus erythematosus: risk factors for increased carotid intima-media thickness in the atherosclerosis prevention in pediatric lupus erythematosus cohort. Arthritis Rheum 2009; 60(5): 1496-507.
[http://dx.doi.org/10.1002/art.24469] [PMID: 19404953]
[99]
Ramzy D, Tumiati LC, Tepperman E, et al. Dual immunosuppression enhances vasomotor injury: interactive effect between endothelin-1 and nitric oxide bioavailability. J Thorac Cardiovasc Surg 2008; 135(4): 938-44.
[http://dx.doi.org/10.1016/j.jtcvs.2007.09.075] [PMID: 18374784]
[100]
Schäfer SC, Wallerath T, Closs EI, et al. Dexamethasone suppresses eNOS and CAT-1 and induces oxidative stress in mouse resistance arterioles. Am J Physiol Heart Circ Physiol 2005; 288(1): H436-44.
[http://dx.doi.org/10.1152/ajpheart.00587.2004] [PMID: 15598872]
[101]
Verhoeven F, Prati C, Maguin-Gaté K, Wendling D, Demougeot C. Glucocorticoids and endothelial function in inflammatory diseases: focus on rheumatoid arthritis. Arthritis Res Ther 2016; 18(1): 258.
[http://dx.doi.org/10.1186/s13075-016-1157-0] [PMID: 27814748]
[102]
Boumpas DT. A novel action of glucocorticoids--NF-kappa B inhibition. Br J Rheumatol 1996; 35(8): 709-10.
[http://dx.doi.org/10.1093/rheumatology/35.8.709] [PMID: 8761180]
[103]
van de Stolpe A, Caldenhoven E, Raaijmakers JA, van der Saag PT, Koenderman L. Glucocorticoid-mediated repression of intercellular adhesion molecule-1 expression in human monocytic and bronchial epithelial cell lines. Am J Respir Cell Mol Biol 1993; 8(3): 340-7.
[http://dx.doi.org/10.1165/ajrcmb/8.3.340] [PMID: 8095395]
[104]
Pamukcu B, Lip GY, Shantsila E. The nuclear factor--kappa B pathway in atherosclerosis: a potential therapeutic target for atherothrombotic vascular disease. Thromb Res 2011; 128(2): 117-23.
[http://dx.doi.org/10.1016/j.thromres.2011.03.025] [PMID: 21636112]
[105]
Asai K, Funaki C, Hayashi T, et al. Dexamethasone-induced suppression of aortic atherosclerosis in cholesterol-fed rabbits. Possible mechanisms. Arterioscler Thromb 1993; 13(6): 892-9.
[http://dx.doi.org/10.1161/01.ATV.13.6.892] [PMID: 8499410]
[106]
Sarnes E, Crofford L, Watson M, Dennis G, Kan H, Bass D. Incidence and US costs of corticosteroid-associated adverse events: a systematic literature review. Clin Ther 2011; 33(10): 1413-32.
[http://dx.doi.org/10.1016/j.clinthera.2011.09.009] [PMID: 21999885]
[107]
Kaiser R, Cleveland CM, Criswell LA. Risk and protective factors for thrombosis in systemic lupus erythematosus: results from a large, multi-ethnic cohort. Ann Rheum Dis 2009; 68(2): 238-41.
[http://dx.doi.org/10.1136/ard.2008.093013] [PMID: 18782792]
[108]
Jung H, Bobba R, Su J, et al. The protective effect of antimalarial drugs on thrombovascular events in systemic lupus erythematosus. Arthritis Rheum 2010; 62(3): 863-8.
[http://dx.doi.org/10.1002/art.27289] [PMID: 20131232]
[109]
Ruiz-Irastorza G, Egurbide MV, Pijoan JI, et al. Effect of antimalarials on thrombosis and survival in patients with systemic lupus erythematosus. Lupus 2006; 15(9): 577-83.
[http://dx.doi.org/10.1177/0961203306071872] [PMID: 17080912]
[110]
Selzer F, Sutton-Tyrrell K, Fitzgerald S, Tracy R, Kuller L, Manzi S. Vascular stiffness in women with systemic lupus erythematosus. Hypertension 2001; 37(4): 1075-82.
[http://dx.doi.org/10.1161/01.HYP.37.4.1075] [PMID: 11304506]
[111]
Durcan L, Winegar DA, Connelly MA, Otvos JD, Magder LS, Petri M. Longitudinal evaluation of lipoprotein variables in systemic lupus erythematosus reveals adverse changes with disease activity and prednisone and more favorable profiles with hydroxychloroquine therapy. J Rheumatol 2016; 43(4): 745-50.
[http://dx.doi.org/10.3899/jrheum.150437] [PMID: 26834214]
[112]
Rahman P, Gladman DD, Urowitz MB, Yuen K, Hallett D, Bruce IN. The cholesterol lowering effect of antimalarial drugs is enhanced in patients with lupus taking corticosteroid drugs. J Rheumatol 1999; 26(2): 325-30.
[PMID: 9972966]
[113]
Virdis A, Tani C, Duranti E, et al. Early treatment with hydroxychloroquine prevents the development of endothelial dysfunction in a murine model of systemic lupus erythematosus. Arthritis Res Ther 2015; 17: 277.
[http://dx.doi.org/10.1186/s13075-015-0790-3] [PMID: 26444671]
[114]
Sacre K, Criswell LA, McCune JM. Hydroxychloroquine is associated with impaired interferon-alpha and tumor necrosis factor-alpha production by plasmacytoid dendritic cells in systemic lupus erythematosus. Arthritis Res Ther 2012; 14(3): R155.
[http://dx.doi.org/10.1186/ar3895] [PMID: 22734582]
[115]
Frangou E, Chrysanthopoulou A, Mitsios A, et al. REDD1/autophagy pathway promotes thromboinflammation and fibrosis in human systemic lupus erythematosus (SLE) through NETs decorated with tissue factor (TF) and interleukin-17A (IL-17A). Ann Rheum Dis 2019; 78(2): 238-48.
[http://dx.doi.org/10.1136/annrheumdis-2018-213181] [PMID: 30563869]
[116]
Teixeira V, Tam LS. Novel insights in systemic lupus erythematosus and atherosclerosis. Front Med (Lausanne) 2018; 4: 262.
[http://dx.doi.org/10.3389/fmed.2017.00262] [PMID: 29435447]
[117]
Espinola RG, Pierangeli SS, Gharavi AE, Harris EN. Hydroxychloroquine reverses platelet activation induced by human IgG antiphospholipid antibodies. Thromb Haemost 2002; 87(3): 518-22.
[http://dx.doi.org/10.1055/s-0037-1613033] [PMID: 11916085]
[118]
van Leuven SI, Mendez-Fernandez YV, Wilhelm AJ, et al. Mycophenolate mofetil but not atorvastatin attenuates atherosclerosis in lupus-prone LDLr(-/-) mice. Ann Rheum Dis 2012; 71(3): 408-14.
[http://dx.doi.org/10.1136/annrheumdis-2011-200071] [PMID: 21953346]
[119]
Romero F, Rodríguez-Iturbe B, Pons H, et al. Mycophenolate mofetil treatment reduces cholesterol-induced atherosclerosis in the rabbit. Atherosclerosis 2000; 152(1): 127-33.
[http://dx.doi.org/10.1016/S0021-9150(99)00458-X] [PMID: 10996347]
[120]
van Leuven SI, van Wijk DF, Volger OL, et al. Mycophenolate mofetil attenuates plaque inflammation in patients with symptomatic carotid artery stenosis. Atherosclerosis 2010; 211(1): 231-6.
[http://dx.doi.org/10.1016/j.atherosclerosis.2010.01.043] [PMID: 20202636]
[121]
Kiani AN, Magder LS, Petri M. Mycophenolate mofetil (MMF) does not slow the progression of subclinical atherosclerosis in SLE over 2 years. Rheumatol Int 2012; 32(9): 2701-5.
[http://dx.doi.org/10.1007/s00296-011-2048-y] [PMID: 21792642]
[122]
Sazliyana S, Mohd Shahrir MS, Kong CT, Tan HJ, Hamidon BB, Azmi MT. Implications of immunosuppressive agents in cardiovascular risks and carotid intima media thickness among lupus nephritis patients. Lupus 2011; 20(12): 1260-6.
[http://dx.doi.org/10.1177/0961203311411347] [PMID: 21844115]
[123]
Ridker PM, Everett BM, Pradhan A, et al. Low-dose methotrexate for the prevention of atherosclerotic events. N Engl J Med 2019; 380(8): 752-62.
[http://dx.doi.org/10.1056/NEJMoa1809798] [PMID: 30415610]
[124]
Micha R, Imamura F, Wyler von Ballmoos M, et al. Systematic review and meta-analysis of methotrexate use and risk of cardiovascular disease. Am J Cardiol 2011; 108(9): 1362-70.
[http://dx.doi.org/10.1016/j.amjcard.2011.06.054] [PMID: 21855836]
[125]
Ahmad Y, Shelmerdine J, Bodill H, et al. Subclinical atherosclerosis in systemic lupus erythematosus (SLE): the relative contribution of classic risk factors and the lupus phenotype. Rheumatology (Oxford) 2007; 46(6): 983-8.
[http://dx.doi.org/10.1093/rheumatology/kem002] [PMID: 17384179]
[126]
Ho KT, Ahn CW, Alarcón GS, et al. Systemic lupus erythematosus in a multiethnic cohort (LUMINA): XXVIII. Factors predictive of thrombotic events. Rheumatology (Oxford) 2005; 44(10): 1303-7.
[http://dx.doi.org/10.1093/rheumatology/kei014] [PMID: 16030085]
[127]
Oryoji K, Kiyohara C, Horiuchi T, et al. Reduced carotid intima-media thickness in systemic lupus erythematosus patients treated with cyclosporine A. Mod Rheumatol 2014; 24(1): 86-92.
[http://dx.doi.org/10.3109/14397595.2013.852838] [PMID: 24261763]
[128]
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.
[http://dx.doi.org/10.1136/annrheumdis-2019-215089] [PMID: 30926722]
[129]
Benvenuti F, Gatto M, Larosa M, Iaccarino L, Punzi L, Doria A. Cardiovascular risk factors, burden of disease and preventive strategies in patients with systemic lupus erythematosus: a literature review. Expert Opin Drug Saf 2015; 14(9): 1373-85.
[http://dx.doi.org/10.1517/14740338.2015.1073259] [PMID: 26212119]
[130]
Ait-Oufella H, Herbin O, Bouaziz JD, et al. B cell depletion reduces the development of atherosclerosis in mice. J Exp Med 2010; 207(8): 1579-87.
[http://dx.doi.org/10.1084/jem.20100155] [PMID: 20603314]
[131]
Koulouri V, Koutsilieris M, Mavragani CP. B cells and atherosclerosis in systemic lupus erythematosus. Expert Rev Clin Immunol 2019; 15(4): 417-29.
[http://dx.doi.org/10.1080/1744666X.2019.1571411] [PMID: 30652925]
[132]
Kyaw T, Cui P, Tay C, et al. BAFF receptor mAb treatment ameliorates development and progression of atherosclerosis in hyperlipidemic ApoE(-/-) mice. PLoS One 2013; 8(4): e60430.
[http://dx.doi.org/10.1371/journal.pone.0060430] [PMID: 23560095]
[133]
Kyaw T, Tay C, Hosseini H, et al. Depletion of B2 but not B1a B cells in BAFF receptor-deficient ApoE mice attenuates atherosclerosis by potently ameliorating arterial inflammation. PLoS One 2012; 7(1): e29371.
[http://dx.doi.org/10.1371/journal.pone.0029371] [PMID: 22238605]
[134]
Kahn P, Ramanujam M, Bethunaickan R, et al. Prevention of murine antiphospholipid syndrome by BAFF blockade. Arthritis Rheum 2008; 58(9): 2824-34.
[http://dx.doi.org/10.1002/art.23764] [PMID: 18759321]
[135]
Sciascia S, Rubini E, Radin M, Cecchi I, Rossi D, Roccatello D. Anticardiolipin and anti-beta 2 glycoprotein-I antibodies disappearance in patients with systemic lupus erythematosus and antiphospholipid syndrome while on belimumab. Ann Rheum Dis 2018; 77(11): 1694-5.
[http://dx.doi.org/10.1136/annrheumdis-2018-213496] [PMID: 29776976]
[136]
Parodis I, Gomez A, Emamikia S, Chatzidionysiou K. Established organ damage reduces belimumab efficacy in systemic lupus erythematosus. Ann Rheum Dis 2019; 78(7): 1006-7.
[http://dx.doi.org/10.1136/annrheumdis-2018-214880] [PMID: 30610063]
[137]
Parodis I, Johansson P, Gomez A, Soukka S, Emamikia S, Chatzidionysiou K. Predictors of low disease activity and clinical remission following belimumab treatment in systemic lupus erythematosus. Rheumatology (Oxford) 2019; 58(12): 2170-6.
[http://dx.doi.org/10.1093/rheumatology/kez191] [PMID: 31157891]
[138]
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.
[http://dx.doi.org/10.1016/j.autrev.2017.02.005] [PMID: 28216072]
[139]
Casey KA, Guo X, Smith MA, et al. Type I interferon receptor blockade with anifrolumab corrects innate and adaptive immune perturbations of SLE. Lupus Sci Med 2018; 5(1): e000286.
[PMID: 30538817]
[140]
Cheung TT, Tsoi MF, Cheung BMY. SAT0099 effect of tnf inhibitors on subclinical atherosclerosis in patients with rheumatoid arthritis: A meta-analysis. Ann Rheu Dis 2015; 74(2): 685.
[http://dx.doi.org/10.1136/annrheumdis-2015-eular.5424]
[141]
Toloza SM, Uribe AG, McGwin G Jr, et al. Systemic lupus erythematosus in a multiethnic US cohort (LUMINA). XXIII. Baseline predictors of vascular events. Arthritis Rheum 2004; 50(12): 3947-57.
[http://dx.doi.org/10.1002/art.20622] [PMID: 15593203]
[142]
Koenig KF, Ribi C, Radosavac M, Zulewski H, Trendelenburg M. Swiss SLE cohort study (SSCS). Prevalence of vascular disease in systemic lupus erythematosus compared with type-1 diabetes mellitus: a cross-sectional study of two cohorts. Lupus 2015; 24(1): 58-65.
[http://dx.doi.org/10.1177/0961203314550223] [PMID: 25182169]
[143]
Becker-Merok A, Nossent J. Prevalence, predictors and outcome of vascular damage in systemic lupus erythematosus. Lupus 2009; 18(6): 508-15.
[http://dx.doi.org/10.1177/0961203308099233] [PMID: 19395452]
[144]
Barbhaiya M, Feldman CH, Guan H, et al. Race/ethnicity and cardiovascular events among patients with systemic lupus erythematosus. Arthritis Rheumatol 2017; 69(9): 1823-31.
[http://dx.doi.org/10.1002/art.40174] [PMID: 28598016]
[145]
Ward MM. Outcomes of hospitalizations for myocardial infarctions and cerebrovascular accidents in patients with systemic lupus erythematosus. Arthritis Rheum 2004; 50(10): 3170-6.
[http://dx.doi.org/10.1002/art.20556] [PMID: 15476215]
[146]
Ando T, Adegbala O, Akintoye E, et al. Acute myocardial infarction outcomes in systemic lupus erythematosus (from the nationwide inpatient sample). Am J Cardiol 2019; 123(2): 227-32.
[http://dx.doi.org/10.1016/j.amjcard.2018.09.043] [PMID: 30424870]
[147]
Maksimowicz-McKinnon K, Selzer F, Manzi S, et al. Poor 1-year outcomes after percutaneous coronary interventions in systemic lupus erythematosus: report from the national heart, lung, and blood institute dynamic registry. Circ Cardiovasc Interv 2008; 1(3): 201-8.
[http://dx.doi.org/10.1161/CIRCINTERVENTIONS.108.788745] [PMID: 20031679]
[148]
Björnådal L, Yin L, Granath F, Klareskog L, Ekbom A. Cardiovascular disease a hazard despite improved prognosis in patients with systemic lupus erythematosus: results from a Swedish population based study 1964-95. J Rheumatol 2004; 31(4): 713-9.
[PMID: 15088296]
[149]
Lin CY, Shih CC, Yeh CC, Chou WH, Chen TL, Liao CC. Increased risk of acute myocardial infarction and mortality in patients with systemic lupus erythematosus: two nationwide retrospective cohort studies. Int J Cardiol 2014; 176(3): 847-51.
[http://dx.doi.org/10.1016/j.ijcard.2014.08.006] [PMID: 25156834]
[150]
Arkema EV, Svenungsson E, Von Euler M, Sjöwall C, Simard JF. Stroke in systemic lupus erythematosus: a Swedish population-based cohort study. Ann Rheum Dis 2017; 76(9): 1544-9.
[http://dx.doi.org/10.1136/annrheumdis-2016-210973] [PMID: 28400384]
[151]
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.
[http://dx.doi.org/10.1080/03009740902776927] [PMID: 19296403]
[152]
Holmqvist M, Simard JF, Asplund K, Arkema EV. Stroke in systemic lupus erythematosus: a meta-analysis of population-based cohort studies. RMD Open 2015; 1(1): e000168.
[http://dx.doi.org/10.1136/rmdopen-2015-000168] [PMID: 26719816]
[153]
Nikolopoulos D, Fanouriakis A, Boumpas D. Cerebrovascular events in systemic lupus erythematosus: Diagnosis and management. Mediterr J Rheumatol 2019; 30(1): 7-15.
[http://dx.doi.org/10.31138/mjr.30.1.7]
[154]
Rossides M, Simard JF, Svenungsson E, von Euler M, Arkema EV. Mortality and functionality after stroke in patients with systemic lupus erythematosus. J Rheumatol 2017; 44(11): 1590-6.
[http://dx.doi.org/10.3899/jrheum.170241] [PMID: 28916550]
[155]
Erdozain JG, Villar I, Nieto J, Ruiz-Irastorza G. Peripheral arterial disease in systemic lupus erythematosus: prevalence and risk factors. J Rheumatol 2014; 41(2): 310-7.
[http://dx.doi.org/10.3899/jrheum.130817] [PMID: 24429176]
[156]
June RR, Scalzi LV. Peripheral vascular disease in systemic lupus patients. J Clin Rheumatol 2013; 19(7): 367-72.
[http://dx.doi.org/10.1097/RHU.0000000000000017] [PMID: 24048099]
[157]
Hassan AA, Habib HM, Eissa AA. Peripheral arterial disease in patients with systemic lupus erythematosus: a prospective controlled study. Int J Rheum Dis 2013; 16(3): 319-24.
[http://dx.doi.org/10.1111/1756-185x.12025] [PMID: 23981754]
[158]
Chuang YW, Yu MC, Lin CL, Yu TM, Shu KH, Kao CH. Risk of peripheral arterial occlusive disease in patients with systemic lupus erythematosus: a nationwide population-based cohort study. Medicine (Baltimore) 2015; 94(46): e2121.
[http://dx.doi.org/10.1097/MD.0000000000002121] [PMID: 26579830]
[159]
Chung CP, Oeser A, Avalos I, Raggi P, Stein CM. Cardiovascular risk scores and the presence of subclinical coronary artery atherosclerosis in women with systemic lupus erythematosus. Lupus 2006; 15(9): 562-9.
[http://dx.doi.org/10.1177/0961203306071870] [PMID: 17080910]
[160]
Sivakumaran J, Harvey P, Omar A, et al. 291 Assessment of the QRISK2, QRISK3, SLE cardiovascular risk equation, modified framingham and framingham risk calculators as predictors of cardiovascular disease events in systemic lupus erythematosus. Lupus Science. Medicine (Baltimore) 2019; 6(Suppl. 1): A211.
[161]
Hippisley-Cox J, Coupland C, Brindle P. Development and validation of QRISK3 risk prediction algorithms to estimate future risk of cardiovascular disease: prospective cohort study. BMJ 2017; 357: j2099.
[http://dx.doi.org/10.1136/bmj.j2099] [PMID: 28536104]
[162]
Piepoli MF, Hoes AW, Agewall S, et al. 2016 European guidelines on cardiovascular disease prevention in clinical practice: the sixth joint task force of the European society of cardiology and other societies on cardiovascular disease prevention in clinical practice (constituted by representatives of 10 societies and by invited experts) developed with the special contribution of the European association for cardiovascular prevention & rehabilitation (EACPR). Eur Heart J 2016; 37(29): 2315-81.
[http://dx.doi.org/10.1093/eurheartj/ehw106] [PMID: 27222591]
[163]
Urowitz MB, Ibañez D, Su J, Gladman DD. Modified framingham risk factor score for systemic lupus Erythematosus. J Rheumatol 2016; 43(5): 875-9.
[http://dx.doi.org/10.3899/jrheum.150983] [PMID: 26879352]
[164]
Petri M, Magder L. Systemic lupus erythematosus cardiovascular risk equation meeting abs 2012 available from 2012.https://acrabstracts.org/abstract/systemic-lupus-erythematosus-cardiovascular-risk-equation/
[165]
Hadamitzky M, Freissmuth B, Meyer T, et al. Prognostic value of coronary computed tomographic angiography for prediction of cardiac events in patients with suspected coronary artery disease. JACC Cardiovasc Imaging 2009; 2(4): 404-11.
[http://dx.doi.org/10.1016/j.jcmg.2008.11.015] [PMID: 19580721]
[166]
Kiani AN, Magder LS, Post WS, et al. Coronary calcification in SLE: comparison with the Multi-Ethnic Study of Atherosclerosis. Rheumatology (Oxford) 2015; 54(11): 1976-81.
[http://dx.doi.org/10.1093/rheumatology/kev198] [PMID: 26106213]
[167]
Petri MA, Kiani AN, Post W, Christopher-Stine L, Magder LS. Lupus Atherosclerosis Prevention Study (LAPS). Ann Rheum Dis 2011; 70(5): 760-5.
[http://dx.doi.org/10.1136/ard.2010.136762] [PMID: 21177297]
[168]
Nagata M, Kato S, Kitagawa K, et al. Diagnostic accuracy of 1.5-T unenhanced whole-heart coronary MR angiography performed with 32-channel cardiac coils: initial single-center experience. Radiology 2011; 259(2): 384-92.
[http://dx.doi.org/10.1148/radiol.11101323] [PMID: 21406635]
[169]
Płazak W, Gryga K, Sznajd J, Pasowicz M, Musiał J, Podolec P. Myocardial ischaemia in systemic lupus erythematosus: detection and clinical relevance. Kardiol Pol 2011; 69(11): 1129-36.
[PMID: 22090220]
[170]
Varma N, Hinojar R, D’Cruz D, et al. Coronary vessel wall contrast enhancement imaging as a potential direct marker of coronary involvement: integration of findings from CAD and SLE patients. JACC Cardiovasc Imaging 2014; 7(8): 762-70.
[http://dx.doi.org/10.1016/j.jcmg.2014.03.012] [PMID: 25051945]
[171]
O’Leary DH, Polak JF, Kronmal RA, Manolio TA, Burke GL, Wolfson SK Jr. Carotid-artery intima and media thickness as a risk factor for myocardial infarction and stroke in older adults. N Engl J Med 1999; 340(1): 14-22.
[http://dx.doi.org/10.1056/NEJM199901073400103] [PMID: 9878640]
[172]
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.
[http://dx.doi.org/10.1016/j.jbspin.2017.12.009] [PMID: 29288864]
[173]
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.
[http://dx.doi.org/10.1161/ATVBAHA.109.198424] [PMID: 20150560]
[174]
Hadi HA, Carr CS, Al Suwaidi J. Endothelial dysfunction: cardiovascular risk factors, therapy, and outcome. Vasc Health Risk Manag 2005; 1(3): 183-98.
[PMID: 17319104]
[175]
Ghiadoni L, Salvetti M, Muiesan ML, Taddei S. Evaluation of endothelial function by flow mediated dilation: methodological issues and clinical importance. High Blood Press Cardiovasc Prev 2015; 22(1): 17-22.
[http://dx.doi.org/10.1007/s40292-014-0047-2] [PMID: 24619864]
[176]
Lima DS, Sato EI, Lima VC, Miranda F Jr, Hatta FH. Brachial endothelial function is impaired in patients with systemic lupus erythematosus. J Rheumatol 2002; 29(2): 292-7.
[PMID: 11842823]
[177]
Mak A, Kow NY, Schwarz H, Gong L, Tay SH, Ling LH. Endothelial dysfunction in systemic lupus erythematosus - a case-control study and an updated meta-analysis and meta-regression. Sci Rep 2017; 7(1): 7320.
[http://dx.doi.org/10.1038/s41598-017-07574-1] [PMID: 28779080]
[178]
Korsten P, Patschan D, Henze E, Niewold TB, Müller GA, Patschan S. Dynamics of pulse wave velocity and vascular augmentation index in association with endothelial progenitor cells in SLE. Lupus Sci Med 2016; 3(1): e000185.
[http://dx.doi.org/10.1136/lupus-2016-000185] [PMID: 28176918]
[179]
Tso TK, Huang WN, Huang HY, Chang CK. Association of brachial-ankle pulse wave velocity with cardiovascular risk factors in systemic lupus erythematosus. Lupus 2005; 14(11): 878-83.
[http://dx.doi.org/10.1191/0961203305lu2234oa] [PMID: 16335579]
[180]
Vázquez-Del Mercado M, Perez-Vazquez FJ, Gomez-Bañuelos E, et al. Subclinical parameters of arterial stiffness and arteriosclerosis correlate with QRISK3 in systemic lupus erythematosus. PLoS One 2018; 13(12): e0207520.
[http://dx.doi.org/10.1371/journal.pone.0207520] [PMID: 30517121]
[181]
McMahon M, Skaggs BJ, Grossman JM, et al. A panel of biomarkers is associated with increased risk of the presence and progression of atherosclerosis in women with systemic lupus erythematosus. Arthritis Rheumatol 2014; 66(1): 130-9.
[http://dx.doi.org/10.1002/art.38204] [PMID: 24449580]
[182]
Lewandowski LB, Kaplan MJ. Update on cardiovascular disease in lupus. Curr Opin Rheumatol 2016; 28(5): 468-76.
[http://dx.doi.org/10.1097/BOR.0000000000000307] [PMID: 27227346]
[183]
Hughes MM, O’Neill LAJ. Metabolic regulation of NLRP3. Immunol Rev 2018; 281(1): 88-98.
[http://dx.doi.org/10.1111/imr.12608] [PMID: 29247992]
[184]
Kahlenberg JM, Kaplan MJ. The inflammasome and lupus: another innate immune mechanism contributing to disease pathogenesis? Curr Opin Rheumatol 2014; 26(5): 475-81.
[http://dx.doi.org/10.1097/BOR.0000000000000088] [PMID: 24992143]
[185]
Oesterle A, Bowman MA. S100A12 and the S100/calgranulins: emerging biomarkers for atherosclerosis and possibly therapeutic targets. Arterioscler Thromb Vasc Biol 2015; 35(12): 2496-507.
[http://dx.doi.org/10.1161/ATVBAHA.115.302072] [PMID: 26515415]
[186]
Baptista D, Mach F, Brandt KJ. Follicular regulatory T cell in atherosclerosis. J Leukoc Biol 2018; 104(5): 925-30.
[http://dx.doi.org/10.1002/JLB.MR1117-469R] [PMID: 30134501]
[187]
Chen Y, Zhang L, Huang H, et al. Association of OX40 and OX40L gene polymorphisms with acute coronary syndrome in a Han Chinese population. DNA Cell Biol 2011; 30(8): 597-602.
[http://dx.doi.org/10.1089/dna.2010.1201] [PMID: 21476935]
[188]
Barta Z, Harrison MJ, Wangrangsimakul T, et al. Health-related quality of life, smoking and carotid atherosclerosis in white British women with systemic lupus erythematosus. Lupus 2010; 19(3): 231-8.
[http://dx.doi.org/10.1177/0961203309351032] [PMID: 20007814]
[189]
dos Reis-Neto ET, da Silva AE, Monteiro CM, de Camargo LM, Sato EI. Supervised physical exercise improves endothelial function in patients with systemic lupus erythematosus. Rheumatology (Oxford) 2013; 52(12): 2187-95.
[http://dx.doi.org/10.1093/rheumatology/ket283] [PMID: 23970541]
[190]
Wright SA, O’Prey FM, McHenry MT, et al. A randomised interventional trial of omega-3-polyunsaturated fatty acids on endothelial function and disease activity in systemic lupus erythematosus. Ann Rheum Dis 2008; 67(6): 841-8.
[http://dx.doi.org/10.1136/ard.2007.077156] [PMID: 17875549]
[191]
Tu H, Li Q, Xiang S, et al. Dual effects of statins therapy in systemic lupus erythematosus and SLE-related atherosclerosis: the potential role for regulatory T cells. Atherosclerosis 2012; 222(1): 29-33.
[http://dx.doi.org/10.1016/j.atherosclerosis.2012.02.023] [PMID: 22417842]
[192]
Norby GE, Holme I, Fellström B, et al. Effect of fluvastatin on cardiac outcomes in kidney transplant patients with systemic lupus erythematosus: a randomized placebo-controlled study. Arthritis Rheum 2009; 60(4): 1060-4.
[http://dx.doi.org/10.1002/art.24379] [PMID: 19333947]
[193]
Yu HH, Chen PC, Yang YH, et al. Statin reduces mortality and morbidity in systemic lupus erythematosus patients with hyperlipidemia: A nationwide population-based cohort study. Atherosclerosis 2015; 243(1): 11-8.
[http://dx.doi.org/10.1016/j.atherosclerosis.2015.08.030] [PMID: 26342937]
[194]
Ardoin SP, Schanberg LE, Sandborg CI, et al. Secondary analysis of APPLE study suggests atorvastatin may reduce atherosclerosis progression in pubertal lupus patients with higher C reactive protein. Ann Rheum Dis 2014; 73(3): 557-66.
[http://dx.doi.org/10.1136/annrheumdis-2012-202315] [PMID: 23436914]
[195]
Plazak W, Gryga K, Dziedzic H, et al. Influence of atorvastatin on coronary calcifications and myocardial perfusion defects in systemic lupus erythematosus patients: a prospective, randomized, double-masked, placebo-controlled study. Arthritis Res Ther 2011; 13(4): R117.
[http://dx.doi.org/10.1186/ar3402] [PMID: 21774822]
[196]
Mok CC, Wong CK, To CH, Lai JP, Lam CS. Effects of rosuvastatin on vascular biomarkers and carotid atherosclerosis in lupus: a randomized, double-blind, placebo-controlled trial. Arthritis Care Res (Hoboken) 2011; 63(6): 875-83.
[http://dx.doi.org/10.1002/acr.20440] [PMID: 21309005]
[197]
Arnaud L, Mathian A, Ruffatti A, et al. Efficacy of aspirin for the primary prevention of thrombosis in patients with antiphospholipid antibodies: an international and collaborative meta-analysis. Autoimmun Rev 2014; 13(3): 281-91.
[http://dx.doi.org/10.1016/j.autrev.2013.10.014] [PMID: 24189281]
[198]
Tektonidou MG, Andreoli L, Limper M, et al. EULAR recommendations for the management of antiphospholipid syndrome in adults. Ann Rheum Dis 2019; 78(10): 1296-304.
[http://dx.doi.org/10.1136/annrheumdis-2019-215213] [PMID: 31092409]
[199]
Fasano S, Pierro L, Pantano I, Iudici M, Valentini G. Longterm hydroxychloroquine therapy and low-dose aspirin may have an additive effectiveness in the primary prevention of cardiovascular events in patients with systemic lupus erythematosus. J Rheumatol 2017; 44(7): 1032-8.
[http://dx.doi.org/10.3899/jrheum.161351] [PMID: 28507183]
[200]
Tao CY, Shang J, Chen T, et al. Impact of antimalarial (AM) on serum lipids in systemic lupus erythematosus (SLE) patients: A systematic review and meta-analysis. Medicine (Baltimore) 2019; 98(14): e15030.
[http://dx.doi.org/10.1097/MD.0000000000015030] [PMID: 30946340]
[201]
Rempenault C, Combe B, Barnetche T, et al. Metabolic and cardiovascular benefits of hydroxychloroquine in patients with rheumatoid arthritis: a systematic review and meta-analysis. Ann Rheum Dis 2018; 77(1): 98-103.
[http://dx.doi.org/10.1136/annrheumdis-2017-211836] [PMID: 28970215]
[202]
Arnett DK, Blumenthal RS, Albert MA, et al. 2019 ACC/AHA guideline on the primary prevention of cardiovascular disease: executive summary: a report of the American college of cardiology/American heart association task force on clinical practice guidelines. J Am Coll Cardiol 2019; 74(10): 1376-414.
[http://dx.doi.org/10.1016/j.jacc.2019.03.009] [PMID: 30894319]
[203]
Giannelou M, Mavragani CP. Cardiovascular disease in systemic lupus erythematosus: A comprehensive update. J Autoimmun 2017; 82: 1-12.
[http://dx.doi.org/10.1016/j.jaut.2017.05.008] [PMID: 28606749]

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