Managing Cardiovascular Risk in Systemic Lupus Erythematosus: Considerations for the Clinician

References

• Kaul A, Gordon C, Crow MK, et al. Systemic lupus erythematosus. Nat Rev Dis Primers. 2016;2(1):16039. doi:10.1038/nrdp.2016.39
   PubMedGoogle Scholar
• 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):221–225. doi:10.1016/0002-9343(76)90431-9
   PubMed Web of Science ®Google Scholar
• Borchers AT, Keen CL, Shoenfeld Y, Gershwin ME. Surviving the butterfly and the wolf: mortality trends in systemic lupus erythematosus. Autoimmun Rev. 2004;3(6):423–453. doi:10.1016/j.autrev.2004.04.002
   PubMed Web of Science ®Google Scholar
• Piga M, Arnaud L. The Main Challenges in Systemic Lupus Erythematosus: where Do We Stand? J Clin Med. 2021;10(2). doi:10.3390/jcm10020243
   PubMed Web of Science ®Google Scholar
• Skaggs BJ, Hahn BH, Mcmahon M. Accelerated atherosclerosis in patients with SLE—mechanisms and management. Nat Rev Rheumatol. 2012;8(4):214–223. doi:10.1038/nrrheum.2012.14
   PubMed Web of Science ®Google Scholar
• 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 Oct. 2001;44(10):2331–2337. doi:10.1002/1529-0131(200110)44:10
   PubMed Web of Science ®Google Scholar
• 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. doi:10.3899/jrheum.150460
   PubMed Web of Science ®Google Scholar
• 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):546–550. doi:10.1016/j.atherosclerosis.2009.03.018
   PubMed Web of Science ®Google Scholar
• Koenig KF, Ribi C, Radosavac M, Zulewski H, Trendelenburg M. 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. doi:10.1177/0961203314550223
   PubMed Web of Science ®Google Scholar
• Katz G, Smilowitz NR, Blazer A, Clancy R, Buyon JP, Berger JS. Systemic Lupus Erythematosus and Increased Prevalence of Atherosclerotic Cardiovascular Disease in Hospitalized Patients. Mayo Clin Proc. 2019;94(8):1436–1443. doi:10.1016/j.mayocp.2019.01.044
   PubMed Web of Science ®Google Scholar
• McMahon M, Hahn BH, Skaggs BJ. Systemic lupus erythematosus and cardiovascular disease: prediction and potential for therapeutic intervention. Expert Rev Clin Immunol. 2011;7(2):227–241. doi:10.1586/eci.10.98
   PubMed Web of Science ®Google Scholar
• Zeller CB, Appenzeller S. Cardiovascular disease in systemic lupus erythematosus: the role of traditional and lupus related risk factors. Curr Cardiol Rev. 2008;4(2):116–122. doi:10.2174/157340308784245775
   PubMedGoogle Scholar
• 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):680–687. doi:10.3899/jrheum.130874
   PubMed Web of Science ®Google Scholar
• Ward MM. Premature morbidity from cardiovascular and cerebrovascular diseases in women with systemic lupus erythematosus. Arthritis Rheum. 1999;42(2):338–346. doi:10.1002/1529-0131(199902)42:2<338::aid-anr17>3.0.co;2-u
   PubMed Web of Science ®Google Scholar
• Shah MA, Shah AM, Krishnan E. Poor Outcomes After Acute Myocardial Infarction in Systemic Lupus Erythematosus. J Rheumatol. 2009;36(3):570–575. doi:10.3899/jrheum.080373
   PubMed Web of Science ®Google Scholar
• Bakshi J, Segura BT, Wincup C, Rahman A. Unmet Needs in the Pathogenesis and Treatment of Systemic Lupus Erythematosus. Clin Rev Allergy Immunol. 2018;55(3):352–367. doi:10.1007/s12016-017-8640-5
   PubMed Web of Science ®Google Scholar
• 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):802–806. doi:10.1136/annrheumdis-2018-214802
   PubMed Web of Science ®Google Scholar
• 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):685–691.
   PubMed Web of Science ®Google Scholar
• Bergkamp SC, Wahadat MJ, Salah A, et al. Dysregulated endothelial cell markers in systemic lupus erythematosus: a systematic review and meta-analysis. J Inflamm. 2023;20(1):18. doi:10.1186/s12950-023-00342-1
   Google Scholar
• Guzmán-Martínez G, Marañón C, Network CR. Immune mechanisms associated with cardiovascular disease in systemic lupus erythematosus: a path to potential biomarkers. Front Immunol. 2022;13:974826. doi:10.3389/fimmu.2022.974826
   PubMed Web of Science ®Google Scholar
• Ding X, Xiang W, He X. IFN-I Mediates Dysfunction of Endothelial Progenitor Cells in Atherosclerosis of Systemic Lupus Erythematosus. Front Immunol. 2020;11:581385. doi:10.3389/fimmu.2020.581385
   PubMed Web of Science ®Google Scholar
• Liu Y, Yu X, Zhang W, Zhang X, Wang M, Ji F. Mechanistic insight into premature atherosclerosis and cardiovascular complications in systemic lupus erythematosus. J Autoimmun. 2022;132:102863. doi:10.1016/j.jaut.2022.102863
   PubMed Web of Science ®Google Scholar
• Tselios K, Sarantopoulos A, Gkougkourelas I, Boura P. T regulatory cells: a promising new target in atherosclerosis. Crit Rev Immunol. 2014;34(5):389–397. doi:10.1615/critrevimmunol.2014010802
   PubMed Web of Science ®Google Scholar
• Liu Y, Kaplan MJ. Cardiovascular disease in systemic lupus erythematosus: an update. Curr Opin Rheumatol. 2018;30(5):441–448. doi:10.1097/BOR.0000000000000528
   PubMed Web of Science ®Google Scholar
• Jackson M, Ahmad Y, Bruce IN, Coupes B, Brenchley PE. Activation of transforming growth factor-beta1 and early atherosclerosis in systemic lupus erythematosus. Arthritis Res Ther. 2006;8(3):R81. doi:10.1186/ar1951
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1016/j.semarthrit.2012.12.002
   PubMed Web of Science ®Google Scholar
• Pope JE, Anderson JJ, Felson DT. A meta-analysis of the effects of nonsteroidal anti-inflammatory drugs on blood pressure. Arch Intern Med. 1993;153(4):477–484.
   PubMedGoogle Scholar
• 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):1413–1432. doi:10.1016/j.clinthera.2011.09.009
   PubMed Web of Science ®Google Scholar
• Tselios K, Gladman DD, Su J, Urowitz M. Impact of the new American College of Cardiology/American Heart Association definition of hypertension on atherosclerotic vascular events in systemic lupus erythematosus. Ann Rheum Dis. 2020;79(5):612–617. doi:10.1136/annrheumdis-2019-216764
   PubMed Web of Science ®Google Scholar
• Tselios K, Koumaras C, Gladman DD, Urowitz MB. Dyslipidemia in systemic lupus erythematosus: just another comorbidity? Semin Arthritis Rheum. Apr. 2016;45(5):604–610. doi:10.1016/j.semarthrit.2015.10.010
   Google Scholar
• Borba EF, Bonfá E. Dyslipoproteinemias in systemic lupus erythematosus: influence of disease, activity, and anticardiolipin antibodies. Lupus. 1997;6(6):533–539. doi:10.1177/096120339700600610
   PubMed Web of Science ®Google Scholar
• 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):2428–2437. doi:10.1002/art.24677
   PubMedGoogle Scholar
• Kip KE, Marroquin OC, Kelley DE, et al. Clinical Importance of Obesity Versus the Metabolic Syndrome in Cardiovascular Risk in Women. Circulation. 2004;109(6):706–713. doi:10.1161/01.cir.0000115514.44135.a8
   PubMed Web of Science ®Google Scholar
• 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. 2006;66(2):208–214. doi:10.1136/ard.2006.054973
   PubMed Web of Science ®Google Scholar
• Kuo CY, Tsai TY, Huang YC. Insulin resistance and serum levels of adipokines in patients with systemic lupus erythematosus: a systematic review and meta-analysis. Lupus. 2020;29(9):1078–1084. doi:10.1177/0961203320935185
   PubMed Web of Science ®Google Scholar
• Anselmino M, Ohrvik J, Malmberg K, Standl E, Rydén L, Investigators EHS. Glucose lowering treatment in patients with coronary artery disease is prognostically important not only in established but also in newly detected diabetes mellitus: a report from the Euro Heart Survey on Diabetes and the Heart. Eur Heart J. 2008;29(2):177–184. doi:10.1093/eurheartj/ehm519
   PubMed Web of Science ®Google Scholar
• Stettler C, Allemann S, Jüni P, et al. Glycemic control and macrovascular disease in types 1 and 2 diabetes mellitus: meta-analysis of randomized trials. Am Heart J. 2006;152(1):27–38. doi:10.1016/j.ahj.2005.09.015
   PubMed Web of Science ®Google Scholar
• Selzer F, Sutton-Tyrrell K, Fitzgerald SG, et al. Comparison of risk factors for vascular disease in the carotid artery and aorta in women with systemic lupus erythematosus. Arthritis Rheum. 2004;50(1):151–159. doi:10.1002/art.11418
   PubMedGoogle Scholar
• 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):708–719. doi:10.1093/aje/kws130
   PubMed Web of Science ®Google Scholar
• 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):1789–1794.
   PubMed Web of Science ®Google Scholar
• Sella EM, Sato EI, Leite WA, Oliveira Filho JA, Barbieri A. Myocardial perfusion scintigraphy and coronary disease risk factors in systemic lupus erythematosus. Ann Rheum Dis. 2003;62(11):1066–1070. doi:10.1136/ard.62.11.1066
   PubMed Web of Science ®Google Scholar
• Quintana P-EG, Serrano R, Pons-Estel BA, Bruce IN. Accelerated atherosclerosis and cardiovascular disease in systemic lupus erythematosus. Revista Colombiana de Reumatología. 2021;1(28):21–30.
   Google Scholar
• 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):130–139. doi:10.1002/art.38204
   PubMed Web of Science ®Google Scholar
• Skaggs BJ, Grossman J, Sahakian L, et al. A Panel of Biomarkers Associates With Increased Risk for Cardiovascular Events in Women With Systemic Lupus Erythematosus. ACR Open Rheumatol. 2021;3(4):209–220. doi:10.1002/acr2.11223
   PubMedGoogle Scholar
• 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):736–745. doi:10.1136/annrheumdis-2019-215089
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1186/ar3759
   PubMed Web of Science ®Google Scholar
• Drosos GC, Vedder D, Houben E, et al. EULAR recommendations for cardiovascular risk management in rheumatic and musculoskeletal diseases, including systemic lupus erythematosus and antiphospholipid syndrome. Ann Rheum Dis. 2022:annrheumdis–202. doi:10.1136/annrheumdis-2021-221733
   Web of Science ®Google Scholar
• Sivakumaran J, Harvey P, Omar A, et al. Assessment of cardiovascular risk tools as predictors of cardiovascular disease events in systemic lupus erythematosus. Lupus Sci Med. 2021;8(1):548. doi:10.1136/lupus-2020-000448
   Web of Science ®Google Scholar
• Quevedo-Abeledo JC, Caceres L, Palazuelos C, Llorca J, González-Gay M, Ferraz-Amaro I. QRISK3 relation to carotid plaque is higher than that of score in patients with systemic lupus erythematosus. Rheumatology. 2022;61(4):1408–1416. doi:10.1093/rheumatology/keab531
   PubMed Web of Science ®Google Scholar
• Quevedo-Abeledo JC, González-Gay M, Ferraz-Amaro I. SCORE2 versus SCORE in patients with systemic lupus erythematosus. Ther Adv Musculoskelet Dis. 2022;14:1759720X221092373. doi:10.1177/1759720X221092373
   PubMed Web of Science ®Google Scholar
• 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):211–217. doi:10.1016/j.jaut.2006.09.008
   PubMed Web of Science ®Google Scholar
• 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):2067–2075. doi:10.1007/s10753-014-9940-z
   PubMed Web of Science ®Google Scholar
• Wang P, Mao YM, Zhao CN, et al. Increased Pulse Wave Velocity in Systemic Lupus Erythematosus: a Meta-Analysis. Angiology. 2018;69(3):228–235. doi:10.1177/0003319717715964
   PubMed Web of Science ®Google Scholar
• 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):878–883. doi:10.1191/0961203305lu2234oa
   PubMed Web of Science ®Google Scholar
• Lertratanakul A, Sun J, Wu PW, et al. Risk factors for changes in carotid intima media thickness and plaque over 5 years in women with systemic lupus erythematosus. Lupus Sci Med. 2021;8(1):548. doi:10.1136/lupus-2021-000548
   Web of Science ®Google Scholar
• 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):835–842. doi:10.1002/art.23196
   PubMedGoogle Scholar
• 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):1025–1032. doi:10.1016/j.amjcard.2013.05.040
   PubMed Web of Science ®Google Scholar
• Nussinovitch U. The Heart in Rheumatic, Autoimmune, and Inflammatory Diseases: Pathophysiology, Clinical Aspects, and Therapeutic Approaches. Academic Press; 2017:xxvi, 739.
   Google Scholar
• Kiani AN, Magder LS, Post WS, et al. Coronary calcification in SLE: comparison with the Multi-Ethnic Study of Atherosclerosis. Rheumatology. 2015;54(11):1976–1981. doi:10.1093/rheumatology/kev198
   PubMed Web of Science ®Google Scholar
• Khan A, Arbab-Zadeh A, Kiani AN, Magder LS, Petri M. Progression of noncalcified and calcified coronary plaque by CT angiography in SLE. Rheumatol Int. 2017;37(1):59–65. doi:10.1007/s00296-016-3615-z
   PubMed Web of Science ®Google Scholar
• Nikpour M, Urowitz M, Ibañez D, Gladman D. Relationship between cardiac symptoms, myocardial perfusion defects and coronary angiography findings in systemic lupus erythematosus. Lupus. 2011;20(3):299–304. doi:10.1177/0961203310381512
   PubMed Web of Science ®Google Scholar
• Kaul MS, Rao SV, Shaw LK, Honeycutt E, Ardoin SP. Association of systemic lupus erythematosus with angiographically defined coronary artery disease: a retrospective cohort study. Arthritis Care Res. 2013;65(2):266–273. doi:10.1002/acr.21782
   Web of Science ®Google Scholar
• Plazak W, Pasowicz M, Kostkiewicz M, et al. Influence of chronic inflammation and autoimmunity on coronary calcifications and myocardial perfusion defects in systemic lupus erythematosus patients. Inflamm Res. 2011;60(10):973–980. doi:10.1007/s00011-011-0358-x
   PubMed Web of Science ®Google Scholar
• Doukky R, Hayes K, Frogge N, et al. Impact of appropriate use on the prognostic value of single-photon emission computed tomography myocardial perfusion imaging. Circulation. 2013;128(15):1634–1643. doi:10.1161/CIRCULATIONAHA.113.002744
   PubMed Web of Science ®Google Scholar
• Burkard T, Trendelenburg M, Daikeler T, et al. The heart in systemic lupus erythematosus – a comprehensive approach by cardiovascular magnetic resonance tomography. PLoS One. 2018;13(10):e0202105. doi:10.1371/journal.pone.0202105
   PubMed Web of Science ®Google Scholar
• Mavrogeni S, Sfikakis PP, Gialafos E, et al. Cardiac tissue characterization and the diagnostic value of cardiovascular magnetic resonance in systemic connective tissue diseases. Arthritis Care Res. 2014;66(1):104–112. doi:10.1002/acr.22181
   PubMed Web of Science ®Google Scholar
• Parel PM, Berg AR, Hong CG, et al. Updates in the Impact of Chronic Systemic Inflammation on Vascular Inflammation by Positron Emission Tomography (PET). Curr Cardiol Rep. 2022;24(4):317–326. doi:10.1007/s11886-022-01651-2
   PubMed Web of Science ®Google Scholar
• Joshi AA, Lerman JB, Dey AK, et al. Association Between Aortic Vascular Inflammation and Coronary Artery Plaque Characteristics in Psoriasis. JAMA Cardiol. 2018;3(10):949–956. doi:10.1001/jamacardio.2018.2769
   PubMed Web of Science ®Google Scholar
• Tselios K, Koumaras C, Urowitz MB, Gladman DD. Do current arterial hypertension treatment guidelines apply to systemic lupus erythematosus patients? A critical appraisal. Semin Arthritis Rheum. 2014;43(4):521–525. doi:10.1016/j.semarthrit.2013.07.007
   PubMed Web of Science ®Google Scholar
• Fanouriakis A, Kostopoulou M, Cheema K, et al. 2019 Update of the Joint European League Against Rheumatism and European Renal Association-European Dialysis and Transplant Association (EULAR/ERA-EDTA) recommendations for the management of lupus nephritis. Ann Rheum Dis. 2020;79(6):713–723. doi:10.1136/annrheumdis-2020-216924
   PubMed Web of Science ®Google Scholar
• Floris A, Piga M, Mangoni AA, Bortoluzzi A, Erre GL, Cauli A. Protective Effects of Hydroxychloroquine against Accelerated Atherosclerosis in Systemic Lupus Erythematosus. Mediators Inflamm. 2018;2018:1–11. doi:10.1155/2018/3424136
   Web of Science ®Google Scholar
• Romero-Díaz J, Vargas-Vóracková F, Kimura-Hayama E, et al. Systemic lupus erythematosus risk factors for coronary artery calcifications. Rheumatology. 2012;51(1):110–119. doi:10.1093/rheumatology/ker307
   PubMed Web of Science ®Google Scholar
• 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):863–868. doi:10.1002/art.27289
   PubMedGoogle Scholar
• 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):408–414. doi:10.1136/annrheumdis-2011-200071
   PubMed Web of Science ®Google Scholar
• 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):231–236. doi:10.1016/j.atherosclerosis.2010.01.043
   PubMed Web of Science ®Google Scholar
• 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):2701–2705. doi:10.1007/s00296-011-2048-y
   PubMed Web of Science ®Google Scholar
• Ridker PM, Everett BM, Thuren T, et al. Antiinflammatory Therapy with Canakinumab for Atherosclerotic Disease. N Engl J Med. 2017;377(12):1119–1131. doi:10.1056/NEJMoa1707914
   PubMed Web of Science ®Google Scholar
• Rocha VZ, Rached FH, Miname MH. Insights into the Role of Inflammation in the Management of Atherosclerosis. J Inflamm Res. 2023;16:2223–2239. doi:10.2147/JIR.S276982
   PubMed Web of Science ®Google Scholar
• Ridker PM, Everett BM, Pradhan A, et al. Low-Dose Methotrexate for the Prevention of Atherosclerotic Events. N Engl J Med. 2019;380(8):752–762. doi:10.1056/NEJMoa1809798
   PubMed Web of Science ®Google Scholar
• Ridker PM, Hennekens CH, Buring JE, Rifai N. C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. N Engl J Med. 2000;342(12):836–843. doi:10.1056/NEJM200003233421202
   PubMed Web of Science ®Google Scholar
• Barbhaiya M, Feldman CH, Guan H, et al. Race/Ethnicity and Cardiovascular Events Among Patients With Systemic Lupus Erythematosus. Arthritis Rheumatol. 2017;69(9):1823–1831. doi:10.1002/art.40174
   PubMed Web of Science ®Google Scholar