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Current Rheumatology Reviews

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ISSN (Print): 1573-3971
ISSN (Online): 1875-6360

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Review Article

Systemic Lupus Erythematosus and Endothelial Dysfunction: A Close Relationship

Author(s): Edoardo Sciatti*, Ilaria Cavazzana, Enrico Vizzardi, Ivano Bonadei, Micaela Fredi, Mara Taraborelli, Romina Ferizi, Marco Metra, Angela Tincani and Franco Franceschini

Volume 15, Issue 3, 2019

Page: [177 - 188] Pages: 12

DOI: 10.2174/1573397115666181126105318

Price: $65

Abstract

Background: Accelerated atherosclerosis, responsible for premature cardiovascular disease, has been estimated to develop or progress in 10% of systemic lupus erythematosus (SLE) patients each year and to be 6-fold more frequent in SLE compared with the general population. The mechanisms underlying accelerated atherosclerosis in SLE are complex and involve classical and “non-classical” cardiovascular risk factors. Subclinical and disseminated atherosclerosis is associated with endothelial dysfunction and arterial stiffness.

Objective: The aim of this review is to analyze the association between SLE and endothelial dysfunction.

Results and Conclusion: Different mechanisms have been proposed to explain the prevalence of endothelial dysfunction in SLE, which are briefly reported in this review: impaired clearance of apoptotic cells, oxidative stress markers, B cell activation with different circulating autoantibodies, different subtypes of T lymphocytes, cytokine cascade. Several studies and meta-analyses show a significant trend towards a prevalence of subclinical accelerated atherosclerosis in patients with SLE compared with healthy controls, since childhood. Based on general considerations, we suggest a multidisciplinary management to assess endothelial dysfunction at the diagnosis of the disease and to periodically search for and treat the traditional cardiovascular risk factors. Prospective studies are needed to confirm the benefits of this management.

Keywords: Endothelial dysfunction, SLE, microvascular, regulatory T cells, angiogenic T cells, T lymphocytes.

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[1]
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.
[http://dx.doi.org/10.1016/j.amjmed.2005.11.034] [PMID: 16887417]
[2]
Cervera R, Khamashta MA, Font J, et al. Morbidity and mortality in systemic lupus erythematosus during a 10-year period: a comparison of early and late manifestations in a cohort of 1,000 patients. Medicine (Baltimore) 2003; 82(5): 299-308.
[http://dx.doi.org/10.1097/01.md.0000091181.93122.55] [PMID: 14530779]
[3]
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]
[4]
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]
[5]
Lee YH, Choi SJ, Ji JD, Song GG. Overall and cause-specific mortality in systemic lupus erythematosus: an updated meta-analysis. Lupus 2016; 25(7): 727-34.
[http://dx.doi.org/10.1177/0961203315627202] [PMID: 26811368]
[6]
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]
[7]
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]
[8]
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]
[9]
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]
[10]
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]
[11]
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]
[12]
Kao AH, Wasko MC, Krishnaswami S, et al. C-reactive protein and coronary artery calcium in asymptomatic women with systemic lupus erythematosus or rheumatoid arthritis. Am J Cardiol 2008; 102(6): 755-60.
[http://dx.doi.org/10.1016/j.amjcard.2008.04.059] [PMID: 18774002]
[13]
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]
[14]
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]
[15]
Enocsson H, Sjöwall C, Kastbom A, et al. Association of serum C-reactive protein levels with lupus disease activity in the absence of measurable interferon-α and a C-reactive protein gene variant. Arthritis Rheum 2014; 66(6): 1568-73.
[http://dx.doi.org/10.1002/art.38408] [PMID: 24574329]
[16]
Mak A, Kow NY. Imbalance between endothelial damage and repair: A gateway to cardiovascular disease in systemic lupus erythematosus. BioMed Res Int 2014.2014178721
[http://dx.doi.org/10.1155/2014/178721] [PMID: 24790989]
[17]
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]
[18]
Kinlay S, Libby P, Ganz P. Endothelial function and coronary artery disease. Curr Opin Lipidol 2001; 12(4): 383-9.
[http://dx.doi.org/10.1097/00041433-200108000-00003] [PMID: 11507322]
[19]
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.
[http://dx.doi.org/10.1182/blood-2003-09-3198] [PMID: 14726373]
[20]
Wigren M, Nilsson J, Kaplan MJ. Pathogenic immunity in systemic lupus erythematosus and atherosclerosis: common mechanisms and possible targets for intervention. J Intern Med 2015; 278(5): 494-506.
[http://dx.doi.org/10.1111/joim.12357] [PMID: 25720452]
[21]
Shao WH, Cohen PL. Disturbances of apoptotic cell clearance in systemic lupus erythematosus. Arthritis Res Ther 2011; 13(1): 202.
[http://dx.doi.org/10.1186/ar3206] [PMID: 21371352]
[22]
Van Vré EA, Ait-Oufella H, Tedgui A, Mallat Z. Apoptotic cell death and efferocytosis in atherosclerosis. Arterioscler Thromb Vasc Biol 2012; 32(4): 887-93.
[http://dx.doi.org/10.1161/ATVBAHA.111.224873] [PMID: 22328779]
[23]
Dichi I, Bregano JW, Simao A, Cecchini R, Eds. Role of oxida-tive stress in chronic diseases. CRC Press 2014; pp. 1-692.
[http://dx.doi.org/10.1201/b16653]
[24]
Shah D, Mahajan N, Sah S, Nath SK, Paudyal B. Oxidative stress and its biomarkers in systemic lupus erythematosus. J Biomed Sci 2014; 21: 23.
[http://dx.doi.org/10.1186/1423-0127-21-23] [PMID: 24636579]
[25]
Morgan PE, Sturgess AD, Davies MJ. Increased levels of serum protein oxidation and correlation with disease activity in systemic lupus erythematosus. Arthritis Rheum 2005; 52(7): 2069-79.
[http://dx.doi.org/10.1002/art.21130] [PMID: 15986354]
[26]
Wang G, Pierangeli SS, Papalardo E, Ansari GAS, Khan MF. Markers of oxidative and nitrosative stress in systemic lupus erythematosus: correlation with disease activity. Arthritis Rheum 2010; 62(7): 2064-72.
[http://dx.doi.org/10.1002/art.27442] [PMID: 20201076]
[27]
Morgan PE, Sturgess AD, Davies MJ. Evidence for chronically elevated serum protein oxidation in systemic lupus erythematosus patients. Free Radic Res 2009; 43(2): 117-27.
[http://dx.doi.org/10.1080/10715760802623896] [PMID: 19096973]
[28]
Marui N, Offermann MK, Swerlick R, et al. Vascular cell adhesion molecule-1 (VCAM-1) gene transcription and expression are regulated through an antioxidant-sensitive mechanism in human vascular endothelial cells. J Clin Invest 1993; 92(4): 1866-74.
[http://dx.doi.org/10.1172/JCI116778] [PMID: 7691889]
[29]
Springer TA. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 1994; 76(2): 301-14.
[http://dx.doi.org/10.1016/0092-8674(94)90337-9] [PMID: 7507411]
[30]
Jiang X, Chen F. The effect of lipid peroxides and superoxide dismutase on systemic lupus erythematosus: a preliminary study. Clin Immunol Immunopathol 1992; 63(1): 39-44.
[http://dx.doi.org/10.1016/0090-1229(92)90091-2] [PMID: 1591881]
[31]
Meroni PL, Borghi MO, Raschi E, Tedesco F. Pathogenesis of antiphospholipid syndrome: understanding the antibodies. Nat Rev Rheumatol 2011; 7(6): 330-9.
[http://dx.doi.org/10.1038/nrrheum.2011.52] [PMID: 21556027]
[32]
Clancy RM. Circulating endothelial cells and vascular injury in systemic lupus erythematosus. Curr Rheumatol Rep 2000; 2(1): 39-43.
[http://dx.doi.org/10.1007/s11926-996-0067-6] [PMID: 11123038]
[33]
Wu M, Barnard J, Kundu S, McCrae KR. A novel pathway of cellular activation mediated by antiphospholipid antibody-induced extracellular vesicles. J Thromb Haemost 2015; 13(10): 1928-40.
[http://dx.doi.org/10.1111/jth.13072] [PMID: 26264622]
[34]
Borghi MO, Raschi E, Grossi C, Chighizola CB, Meroni PL. Toll-like receptor 4 and β2 glycoprotein I interaction on endothelial cells. Lupus 2014; 23(12): 1302-4.
[http://dx.doi.org/10.1177/0961203314536479] [PMID: 25228733]
[35]
Canaud G, Legendre C, Terzi F. AKT/mTORC pathway in antiphospholipid-related vasculopathy: a new player in the game. Lupus 2015; 24(3): 227-30.
[http://dx.doi.org/10.1177/0961203315569336] [PMID: 25631854]
[36]
Hur J, Yang HM, Yoon CH, et al. Identification of a novel role of T cells in postnatal vasculogenesis: characterization of endothelial progenitor cell colonies. Circulation 2007; 116(15): 1671-82.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.107.694778] [PMID: 17909106]
[37]
Rouhl RP, Mertens AE, van Oostenbrugge RJ, et al. Angiogenic T-cells and putative endothelial progenitor cells in hypertension-related cerebral small vessel disease. Stroke 2012; 43(1): 256-8.
[http://dx.doi.org/10.1161/STROKEAHA.111.632208] [PMID: 21980212]
[38]
Rodríguez-Carrio J, Alperi-López M, López P, Alonso-Castro S, Ballina-García FJ, Suárez A. Angiogenic T cells are decreased in rheumatoid arthritis patients. Ann Rheum Dis 2015; 74(5): 921-7.
[http://dx.doi.org/10.1136/annrheumdis-2013-204250] [PMID: 24399233]
[39]
Miao J, Qiu F, Li T, et al. Circulating angiogenic T cells and their subpopulations in patients with systemic lupus erythematosus. Mediators Inflamm 2016.20162842143
[http://dx.doi.org/10.1155/2016/2842143] [PMID: 27065298]
[40]
Manetti M, Pratesi S, Romano E, et al. Angiogenic T cell expansion correlates with severity of peripheral vascular damage in systemic sclerosis. PLoS One 2017; 12(8)e0183102
[http://dx.doi.org/10.1371/journal.pone.0183102] [PMID: 28797111]
[41]
Gerli R, Schillaci G, Giordano A, et al. CD4+CD28- T lymphocytes contribute to early atherosclerotic damage in rheumatoid arthritis patients. Circulation 2004; 109(22): 2744-8.
[http://dx.doi.org/10.1161/01.CIR.0000131450.66017.B3] [PMID: 15159291]
[42]
Weyand CM, Goronzy JJ, Liuzzo G, Kopecky SL, Holmes DR Jr, Frye RL. T-cell immunity in acute coronary syndromes. Mayo Clin Proc 2001; 76(10): 1011-20.
[http://dx.doi.org/10.4065/76.10.1011] [PMID: 11605685]
[43]
Lyssuk EY, Torgashina AV, Soloviev SK, Nassonov EL, Bykovskaia SN. Reduced number and function of CD4+CD25highFoxP3+ regulatory T cells in patients with systemic lupus erythematosus. Adv Exp Med Biol 2007; 601: 113-9.
[http://dx.doi.org/10.1007/978-0-387-72005-0_12] [PMID: 17712998]
[44]
Mor A, Planer D, Luboshits G, et al. Role of naturally occurring CD4+ CD25+ regulatory T cells in experimental atherosclerosis. Arterioscler Thromb Vasc Biol 2007; 27(4): 893-900.
[http://dx.doi.org/10.1161/01.ATV.0000259365.31469.89] [PMID: 17272749]
[45]
Wigren M, Björkbacka H, Andersson L, et al. Low levels of circulating CD4+FoxP3+ T cells are associated with an increased risk for development of myocardial infarction but not for stroke. Arterioscler Thromb Vasc Biol 2012; 32(8): 2000-4.
[http://dx.doi.org/10.1161/ATVBAHA.112.251579] [PMID: 22628434]
[46]
Ait-Oufella H, Salomon BL, Potteaux S, et al. Natural regulatory T cells control the development of atherosclerosis in mice. Nat Med 2006; 12(2): 178-80.
[http://dx.doi.org/10.1038/nm1343] [PMID: 16462800]
[47]
Haque S, Alexander MY, Bruce IN. Endothelial progenitor cells: a new player in lupus? Arthritis Res Ther 2012; 14(1): 203.
[http://dx.doi.org/10.1186/ar3700] [PMID: 22356717]
[48]
Moon JH, Chae MK, Kim KJ, et al. Decreased endothelial progenitor cells and increased serum glycated albumin are independently correlated with plaque-forming carotid artery atherosclerosis in type 2 diabetes patients without documented ischemic disease. Circ J 2012; 76(9): 2273-9.
[http://dx.doi.org/10.1253/circj.CJ-11-1499] [PMID: 22664650]
[49]
Suzuki R, Fukuda N, Katakawa M, et al. Effects of an angiotensin II receptor blocker on the impaired function of endothelial progenitor cells in patients with essential hypertension. Am J Hypertens 2014; 27(5): 695-701.
[http://dx.doi.org/10.1093/ajh/hpt208] [PMID: 24200748]
[50]
Urbich C, Dimmeler S. Risk factors for coronary artery disease, circulating endothelial progenitor cells, and the role of HMG-CoA reductase inhibitors. Kidney Int 2005; 67(5): 1672-6.
[http://dx.doi.org/10.1111/j.1523-1755.2005.00261.x] [PMID: 15840010]
[51]
Tsai NW, Hung SH, Huang CR, et al. The association between circulating endothelial progenitor cells and outcome in different subtypes of acute ischemic stroke. Clin Chim Acta 2014; 427: 6-10.
[http://dx.doi.org/10.1016/j.cca.2013.09.029] [PMID: 24076252]
[52]
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]
[53]
Anderson TJ, Gerhard MD, Meredith IT, et al. Systemic nature of endothelial dysfunction in atherosclerosis. Am J Cardiol 1995; 75(6): 71B-4B.
[http://dx.doi.org/10.1016/0002-9149(95)80017-M] [PMID: 7863979]
[54]
Juonala M, Viikari JS, Laitinen T, et al. Interrelations between brachial endothelial function and carotid intima-media thickness in young adults: the cardiovascular risk in young Finns study. Circulation 2004; 110(18): 2918-23.
[http://dx.doi.org/10.1161/01.CIR.0000147540.88559.00] [PMID: 15505080]
[55]
Linder L, Kiowski W, Bühler FR, Lüscher TF. Indirect evidence for release of endothelium-derived relaxing factor in human forearm circulation in vivo. Blunted response in essential hypertension. Circulation 1990; 81(6): 1762-7.
[http://dx.doi.org/10.1161/01.CIR.81.6.1762] [PMID: 2344673]
[56]
Creager MA, Cooke JP, Mendelsohn ME, et al. Impaired vasodilation of forearm resistance vessels in hypercholesterolemic humans. J Clin Invest 1990; 86(1): 228-34.
[http://dx.doi.org/10.1172/JCI114688] [PMID: 2195060]
[57]
Petrie JR, Ueda S, Morris AD, Murray LS, Elliott HL, Connell JM. How reproducible is bilateral forearm plethysmography? Br J Clin Pharmacol 1998; 45(2): 131-9.
[http://dx.doi.org/10.1046/j.1365-2125.1998.00656.x] [PMID: 9491825]
[58]
Benjamin N, Calver A, Collier J, Robinson B, Vallance P, Webb D. Measuring forearm blood flow and interpreting the responses to drugs and mediators. Hypertension 1995; 25(5): 918-23.
[http://dx.doi.org/10.1161/01.HYP.25.5.918] [PMID: 7737727]
[59]
Cox DA, Vita JA, Treasure CB, et al. Atherosclerosis impairs flow-mediated dilation of coronary arteries in humans. Circulation 1989; 80(3): 458-65.
[http://dx.doi.org/10.1161/01.CIR.80.3.458] [PMID: 2527643]
[60]
Lieberman EH, Gerhard MD, Uehata A, et al. Flow-induced vasodilation of the human brachial artery is impaired in patients <40 years of age with coronary artery disease. Am J Cardiol 1996; 78(11): 1210-4.
[http://dx.doi.org/10.1016/S0002-9149(96)00597-8] [PMID: 8960576]
[61]
Joannides R, Richard V, Haefeli WE, Linder L, Lüscher TF, Thuillez C. Role of basal and stimulated release of nitric oxide in the regulation of radial artery caliber in humans. Hypertension 1995; 26(2): 327-31.
[http://dx.doi.org/10.1161/01.HYP.26.2.327] [PMID: 7635543]
[62]
Corretti MC, Anderson TJ, Benjamin EJ, et al. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. J Am Coll Cardiol 2002; 39(2): 257-65.
[http://dx.doi.org/10.1016/S0735-1097(01)01746-6] [PMID: 11788217]
[63]
Deanfield J, Donald A, Ferri C, et al. Endothelial function and dysfunction. Part I: Methodological issues for assessment in the different vascular beds: a statement by the Working Group on Endothelin and Endothelial Factors of the European Society of Hypertension. J Hypertens 2005; 23(1): 7-17.
[http://dx.doi.org/10.1097/00004872-200501000-00004] [PMID: 15643116]
[64]
Thijssen DH, Black MA, Pyke KE, et al. Assessment of flow-mediated dilation in humans: a methodological and physiological guideline. Am J Physiol Heart Circ Physiol 2011; 300(1): H2-H12.
[http://dx.doi.org/10.1152/ajpheart.00471.2010] [PMID: 20952670]
[65]
Kuvin JT, Patel AR, Sliney KA, et al. Assessment of peripheral vascular endothelial function with finger arterial pulse wave amplitude. Am Heart J 2003; 146(1): 168-74.
[http://dx.doi.org/10.1016/S0002-8703(03)00094-2] [PMID: 12851627]
[66]
Flammer AJ, Lüscher TF. Three decades of endothelium research: from the detection of nitric oxide to the everyday implementation of endothelial function measurements in cardiovascular diseases. Swiss Med Wkly 2010. 140w13122
[http://dx.doi.org/10.4414/smw.2010.13122] [PMID: 21120736]
[67]
Nohria A, Gerhard-Herman M, Creager MA, Hurley S, Mitra D, Ganz P. Role of nitric oxide in the regulation of digital pulse volume amplitude in humans. J Appl Physiol 2006; 101(2): 545-8.
[http://dx.doi.org/10.1152/japplphysiol.01285.2005] [PMID: 16614356]
[68]
Panza JA, Quyyumi AA, Brush JE Jr, Epstein SE. Abnormal endothelium-dependent vascular relaxation in patients with essential hypertension. N Engl J Med 1990; 323(1): 22-7.
[http://dx.doi.org/10.1056/NEJM199007053230105] [PMID: 2355955]
[69]
Shechter M, Issachar A, Marai I, et al. Long-term association of brachial artery flow-mediated vasodilation and cardiovascular events in middle-aged subjects with no apparent heart disease. Int J Cardiol 2009; 134(1): 52-8.
[http://dx.doi.org/10.1016/j.ijcard.2008.01.021] [PMID: 18479768]
[70]
Hirsch L, Shechter A, Feinberg MS, Koren-Morag N, Shechter M. The impact of early compared to late morning hours on brachial endothelial function and long-term cardiovascular events in healthy subjects with no apparent coronary heart disease. Int J Cardiol 2011; 151(3): 342-7.
[http://dx.doi.org/10.1016/j.ijcard.2010.08.069] [PMID: 20832878]
[71]
Yeboah J, Crouse JR, Hsu FC, Burke GL, Herrington DM. Brachial flow-mediated dilation predicts incident cardiovascular events in older adults: the Cardiovascular Health Study. Circulation 2007; 115(18): 2390-7.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.106.678276] [PMID: 17452608]
[72]
Matsuzawa Y, Sugiyama S, Sugamura K, et al. Digital assessment of endothelial function and ischemic heart disease in women. J Am Coll Cardiol 2010; 55(16): 1688-96.
[http://dx.doi.org/10.1016/j.jacc.2009.10.073] [PMID: 20394872]
[73]
Rubinshtein R, Kuvin JT, Soffler M, et al. Assessment of endothelial function by non-invasive peripheral arterial tonometry predicts late cardiovascular adverse events. Eur Heart J 2010; 31(9): 1142-8.
[http://dx.doi.org/10.1093/eurheartj/ehq010] [PMID: 20181680]
[74]
Xu Y, Arora RC, Hiebert BM, et al. Non-invasive endothelial function testing and the risk of adverse outcomes: a systematic review and meta-analysis. Eur Heart J Cardiovasc Imaging 2014; 15(7): 736-46.
[http://dx.doi.org/10.1093/ehjci/jet256] [PMID: 24399339]
[75]
Ahmadi B, Bonakdar ZS, Hashemi SM, Sadrkabir SM, Karimifar M. Endothelial dysfunction in Iranian lupus patients. Rheumatol Int 2011; 31(1): 27-31.
[http://dx.doi.org/10.1007/s00296-009-1212-0] [PMID: 19855975]
[76]
Aizer J, Karlson EW, Chibnik LB, et al. A controlled comparison of brachial artery flow mediated dilation (FMD) and digital pulse amplitude tonometry (PAT) in the assessment of endothelial function in systemic lupus erythematosus. Lupus 2009; 18(3): 235-42.
[http://dx.doi.org/10.1177/0961203308096663] [PMID: 19213862]
[77]
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]
[78]
Chin CW, Chin CY, Ng MX, et al. Endothelial function is associated with myocardial diastolic function in women with systemic lupus erythematosus. Rheumatol Int 2014; 34(9): 1281-5.
[http://dx.doi.org/10.1007/s00296-014-2968-4] [PMID: 24549405]
[79]
Conti F, Spinelli FR, Alessandri C, et al. Subclinical atherosclerosis in systemic lupus erythematosus and antiphospholipid syndrome: focus on β2GPI-specific T cell response. Arterioscler Thromb Vasc Biol 2014; 34(3): 661-8.
[http://dx.doi.org/10.1161/ATVBAHA.113.302680] [PMID: 24436371]
[80]
Cypiene A, Kovaite M, Venalis A, et al. Arterial wall dysfunction in systemic lupus erythematosus. Lupus 2009; 18(6): 522-9.
[http://dx.doi.org/10.1177/0961203308099625] [PMID: 19395454]
[81]
Cypienė A, Dadonienė J, Rugienė R, et al. The influence of mean blood pressure on arterial stiffening and endothelial dysfunction in women with rheumatoid arthritis and systemic lupus erythematosus. Medicina (Kaunas) 2010; 46(8): 522-30.
[http://dx.doi.org/10.3390/medicina46080075] [PMID: 20966628]
[82]
El-Banawy HS, Gaber EW, Maharem DA, Matrawy KA. Angiopoietin-2, endothelial dysfunction and renal involvement in patients with systemic lupus erythematosus. J Nephrol 2012; 25(4): 541-50.
[http://dx.doi.org/10.5301/jn.5000030] [PMID: 21956768]
[83]
El-Magadmi M, Bodill H, Ahmad Y, et al. Systemic lupus erythematosus: an independent risk factor for endothelial dysfunction in women. Circulation 2004; 110(4): 399-404.
[http://dx.doi.org/10.1161/01.CIR.0000136807.78534.50] [PMID: 15262847]
[84]
Ferreira GA, Navarro TP, Telles RW, Andrade LE, Sato EI. Atorvastatin therapy improves endothelial-dependent vasodilation in patients with systemic lupus erythematosus: an 8 weeks controlled trial. Rheumatology (Oxford) 2007; 46(10): 1560-5.
[http://dx.doi.org/10.1093/rheumatology/kem186] [PMID: 17693444]
[85]
Ghiadoni L, Tani C, Bruno RM, et al. Prognostic value of flow-mediated dilation in patients with systemic lupus erythematosus: a pilot prospective cohort study. Atherosclerosis 2014; 236(2): 381-4.
[http://dx.doi.org/10.1016/j.atherosclerosis.2014.07.023] [PMID: 25133352]
[86]
Ghosh P, Kumar A, Kumar S, Aggarwal A, Sinha N, Misra R. Subclinical atherosclerosis and endothelial dysfunction in young South-Asian patients with systemic lupus erythematosus. Clin Rheumatol 2009; 28(11): 1259-65.
[http://dx.doi.org/10.1007/s10067-009-1228-6] [PMID: 19618302]
[87]
Johnson SR, Harvey PJ, Floras JS, et al. Impaired brachial artery endothelium dependent flow mediated dilation in systemic lupus erythematosus: preliminary observations. Lupus 2004; 13(8): 590-3.
[http://dx.doi.org/10.1191/0961203304lu1072oa] [PMID: 15462488]
[88]
Karadag O, Calguneri M, Atalar E, et al. Novel cardiovascular risk factors and cardiac event predictors in female inactive systemic lupus erythematosus patients. Clin Rheumatol 2007; 26(5): 695-9.
[http://dx.doi.org/10.1007/s10067-006-0376-1] [PMID: 16909327]
[89]
Kiss E, Soltesz P, Der H, et al. Reduced flow-mediated vasodilation as a marker for cardiovascular complications in lupus patients. J Autoimmun 2006; 27(4): 211-7.
[http://dx.doi.org/10.1016/j.jaut.2006.09.008] [PMID: 17088047]
[90]
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]
[91]
Mak A, Ling LH, Ho RC, et al. Lumbar spine bone mineral density predicts endothelial reactivity in patients with systemic lupus erythematosus. Clin Exp Rheumatol 2011; 29(2): 261-8.
[PMID: 21385541]
[92]
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]
[93]
Mikołajczyk TP, Osmenda G, Batko B, et al. Heterogeneity of peripheral blood monocytes, endothelial dysfunction and subclinical atherosclerosis in patients with systemic lupus erythematosus. Lupus 2016; 25(1): 18-27.
[http://dx.doi.org/10.1177/0961203315598014] [PMID: 26251402]
[94]
Parker B, Al-Husain A, Pemberton P, et al. Suppression of inflammation reduces endothelial microparticles in active systemic lupus erythematosus. Ann Rheum Dis 2014; 73(6): 1144-50.
[http://dx.doi.org/10.1136/annrheumdis-2012-203028] [PMID: 23644670]
[95]
Piper MK, Raza K, Nuttall SL, et al. Impaired endothelial function in systemic lupus erythematosus. Lupus 2007; 16(2): 84-8.
[http://dx.doi.org/10.1177/0961203306074842] [PMID: 17402363]
[96]
Pramanik AB, Bhattacharyya K, Sinha PK, et al. Study of endothelial dysfunc-tion and its correlation with disease activity in systemic lupus erythematosus patients without conventional cardiovascular risk factors. Indian J Rheumatol 2011; 6: 178-84.
[http://dx.doi.org/10.1016/S0973-3698(11)60204-5]
[97]
Sincer İ, Kurtoğlu E, Yılmaz Çoşkun F, et al. Association between serum total antioxidant status and flow-mediated dilation in patients with systemic lupus erythematosus: an observational study. Anatol J Cardiol 2015; 15(11): 913-8.
[http://dx.doi.org/10.5152/akd.2015.5764] [PMID: 25868041]
[98]
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]
[99]
Stalc M, Tomsic M, Jezovnik MK, Poredos P. Endothelium-dependent and independent dilation capability of peripheral arteries in patients with systemic lupus erythematosus and antiphospholipid syndrome. Clin Exp Rheumatol 2011; 29(4): 616-23.
[PMID: 21813059]
[100]
Svenungsson E, Cederholm A, Jensen-Urstad K, Fei GZ, de Faire U, Frostegård J. Endothelial function and markers of endothelial activation in relation to cardiovascular disease in systemic lupus erythematosus. Scand J Rheumatol 2008; 37(5): 352-9.
[http://dx.doi.org/10.1080/03009740802007514] [PMID: 18666029]
[101]
Taraborelli M, Sciatti E, Bonadei I, et al. Endothelial dysfunction in early systemic lupus ery-thematosus patients and controls without previous cardiovas-cular events. Arthritis Care Res (Hoboken) 2017; 70(9): 1277-83.
[http://dx.doi.org/10.1002/acr.23495] [PMID: 29245186]
[102]
Turner E, Dishy V, Chung CP, et al. Endothelial function in systemic lupus erythematosus: relationship to disease activity, cardiovascular risk factors, corticosteroid therapy, and coronary calcification. Vasc Health Risk Manag 2005; 1(4): 357-60.
[http://dx.doi.org/10.2147/vhrm.2005.1.4.357] [PMID: 17315608]
[103]
Valdivielso P, Gómez-Doblas JJ, Macias M, et al. Lupus-associated endothelial dysfunction, disease activity and arteriosclerosis. Clin Exp Rheumatol 2008; 26(5): 827-33.
[PMID: 19032815]
[104]
Valer P, Paul B, Eugenia B, Camelia B. Annexin A5 as independent predictive biomarker for subclinical atherosclerosis and endothelial dysfunction in systemic lupus erythematosus patients. Clin Lab 2013; 59(3-4): 359-67.
[http://dx.doi.org/10.7754/Clin.Lab.2012.120521] [PMID: 23724626]
[105]
Wright SA, O’Prey FM, Rea DJ, et al. Microcirculatory hemodynamics and endothelial dysfunction in systemic lupus erythematosus. Arterioscler Thromb Vasc Biol 2006; 26(10): 2281-7.
[http://dx.doi.org/10.1161/01.ATV.0000238351.82900.7f] [PMID: 16873725]
[106]
Zhang CY, Lu LJ, Li FH, et al. Evaluation of risk factors that contribute to high prevalence of premature atherosclerosis in Chinese premenopausal systemic lupus erythematosus patients. J Clin Rheumatol 2009; 15(3): 111-6.
[http://dx.doi.org/10.1097/RHU.0b013e31819d8489] [PMID: 19300290]
[107]
Mak A, Liu Y, Ho RC. Endothelium-dependent but not endothelium-independent flow-mediated dilation is significantly reduced in patients with systemic lupus erythematosus without vascular events: a metaanalysis and metaregression. J Rheumatol 2011; 38(7): 1296-303.
[http://dx.doi.org/10.3899/jrheum.101182] [PMID: 21459950]
[108]
Wang DG, Tang XW, Fan Y, et al. Decreased flow-mediated dilatation in patients with systemic lupus erythematosus: a meta-analysis. Inflammation 2014; 37(6): 2067-75.
[http://dx.doi.org/10.1007/s10753-014-9940-z] [PMID: 24906564]

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