DOI: https://doi.org/10.22141/2224-1485.3-4.64-65.2019.177845

Clinical and pathogenetic accents of the cardiovascular comorbidity in systemic lupus erythematosus

Ye.D. Yehudina, I.Yu. Golovach, O.O. Khaniukov

Abstract


The increased incidence of cardiovascular events and subclinical atherosclerosis, confirmed by imaging and vascular function, are proven facts in systemic lupus erythematosus (SLE). Although traditional cardiovascular disease factors, such as smo-
king, dyslipidemia, diabetes mellitus, hypertension, central obesity and hyperhomocysteinemia, are common in patients with SLE, they do not fully explain the high level of ischemic events that have been reported so far, which implies that other factors that are inherent in the disease itself may contribute to an increased risk, including duration of the disease, its activity and chronic course, psychosocial factors, drugs, genetic disorders and altered immunological mechanisms. Although the exact pathogenesis of atherosclerosis in SLE remains poorly understood, the imbalance between endothelial damage and atheroprotection appears to be a central event. Factors leading to endothelial damage in SLE include oxidized low-density lipoproteins (LDL), autoantibodies to endothelial cells and phospholipids, interferons (IFN) type I and neutrophil extracellular traps that act directly or through activation of the type I IFN pathway. Increased oxidative stress, decreased levels of high-density antioxidant lipoproteins (HDL), elevated levels of pro-inflammatory HDL and decreased paraoxonase activity have been associated with elevated levels of oxidized LDL. On the other hand, disorders of atheroprotective mechanisms in SLE include a decrease in the ability of endothelial repair, partially mediated through type I IFN, and a decrease in the production of atheroprotective autoantibodies. This review summarizes the traditional and disease-related risk factors for cardiovascular diseases in chronic autoimmune disorders, with a special focus on SLE.


Keywords


cardiovascular diseases; systemic lupus erythematosus; atherosclerosis; immune dysregulation; risk factors; arterial hypertension

References


Gistera A, Hansson GK. The immunology of atherosclerosis, Nat. Rev. Nephrol. 13 (2017) 368e380 doi: 10.1038/nrneph.2017.51

Avina-Zubieta JA, To F, Vostretsova K, et al. Risk of myocardial infarction and stroke in newly diagnosed systemic lupus erythematosus: a general population- based study. Arthritis Care Res (Hoboken). 2017; 69:849–856. doi: 10.1002/acr.23018

Tselios K, Gladman DD, Su J, et al. Evolution of risk factors for atherosclerotic cardiovascular events in systemic lupus erythematosus: a longterm prospective study. J Rheumatol 2017; 44:1841–1849 doi: 10.3899/jrheum.161121.

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;221-225. https://doi.org/10.1016/0002-9343(76)90431-9

Nossent J, Cikes N, Kiss E, et al, Current causes of death in systemic lupus erythematosus in Europe, 2000-2004: relation to disease activity and damage accrual, Lupus.2007;16:309-317. DOI: 10.1177/0961203307077987

Fernandez-Nebro I, Rua-Figueroa FJ, Lopez-Longo M, et al. Cardiovascular events in systemic lupus erythematosus: a nationwide study in Spain from the RELESSER registry. Medicine.2015;94:1183 doi: 10.1097/MD.0000000000001183.

Tektonidou MG, Kravvariti E, Konstantonis G, et al. Subclinical atherosclerosis in systemic lupus erythematosus: comparable risk with diabetes mellitus and rheumatoid arthritis. Autoimmun Rev. 2017; 16:308–312. https://doi.org/10.1016/j.autrev.2017.01.009

Baragetti A, Ramirez GA, Magnoni M, et al. Disease trends over time and CD4(fl)CCR5(fl) T-cells expansion predict carotid atherosclerosis development in patients with systemic lupus erythematosus. Nutr Metab Cardiovasc Dis. 2018; 28:53–63 doi: 10.1016/j.numecd. 

Boulos D, Koelmeyer RL, Morand EF, Hoi AY. Cardiovascular risk profiles in a lupus cohort: what do different calculators tell us? Lupus Sci Med. 2017;4:e000212 doi: 10.1136/lupus-2017-000212.

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;15:22-37. https://doi.org/10.1016/j.autrev.2015.10.002

Kiani AN, Magder LS, Post WS, et al. Coronary calcification in SLE: comparison with the multi-ethnic study of atherosclerosis. Rheumatol. Oxf. Engl. 2015;54:1976-1981. https://doi.org/10.1093/rheumatology/kev198

El-Magadmi M, Bodill H, Ahmad Y, et al. Systemic lupus erythematosus: an independent risk factor for endothelial dysfunction in women. Circulation.2004;110:399-404 https://doi.org/10.1161/01.CIR.0000136807.78534.50

Morreale B, Mule G, Ferrante A, D'Ignoto F, Cottone S. Early vascular aging in normotensive patients with systemic lupus erythematosus: comparison with young patients having hypertension. Angiology. 2016;67:676-682. https://doi.org/10.1177%2F0003319715613917

El Gamal YM, Elmasry OA, El Hadidi IS, Soliman OK. Proximal aortic stiffness is increased in systemic lupus erythematosus activity in children and adolescents. ISRN Pediatr. 2013; 2013:765253. doi: 10.1155/2013/765253.

Mok CC, Poon WL, Lai JP, et al. Metabolic syndrome, endothelial injury, and subclinical atherosclerosis in patients with systemic lupus erythematosus. Scand. J. Rheumatol. 2010;39:42-49. https://doi.org/10.3109/03009740903046668

Sacre K, Escoubet B, Zennaro MC, Chauveheid MP, Gayat E, Papo T. Overweight is a major contributor to atherosclerosis in systemic lupus erythematosus patients at apparent low risk for cardiovascular disease: a crosssectional controlled study. Medicine. 2015;94:e2177. doi: 10.1097/MD. 0000000000002177

Sanchez-Perez H, Tejera-Segura B, de Vera-Gonzalez A, et al., Insulin resistance in systemic lupus erythematosus patients: contributing factors and relationship with subclinical atherosclerosis. Clin. Exp. Rheumatol. (2017 35: 885-892

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. (Hoboken, NJ). 2014;66:130-139. doi: 10.1002/art.38204

Kiani AN, Post WS, Magder LS, Petri M. Predictors of progression in atherosclerosis over 2 years in systemic lupus erythematosus. Rheumatol. Oxf. Engl.2011;50:2071-9 doi: 10.1093/rheumatology/ker285

Sabio JM, Vargas-Hitos JA, Navarrete-Navarrete N, et al. Prevalence of and factors associated with hypertension in young and old women with systemic lupus erythematosus. J. Rheumatol. 2011;38:1026-1032. DOI: https://doi.org/10.3899/jrheum.101132

Sabio JM, Martinez-Bordonado J, Sanchez-Berna I, et al. Nighttime blood pressure patterns and subclinical atherosclerosis in women with systemic lupus erythematosus, J. Rheumatol. 2015;42:2310-2317. DOI: https://doi.org/10.3899/jrheum.150531

Urowitz MB, Gladman D, Ibanez D, et al. Accumulation of coronary artery disease risk factors over three years: data from an international inception cohort, Arthritis Rheum. 2008; 59:176-180. https://doi.org/10.1002/art.23353

Tselios K, Koumaras C, Gladman DD, Urowitz MB. Dyslipidemia in systemic lupus erythematosus: just another comorbidity? Seminars Arthritis Rheum.2016;45:604-610. https://doi.org/10.1016/j.semarthrit.2015.10.010

Parra S, Vives G, Ferre R, et al. Complement system and small HDL particles are associated with subclinical atherosclerosis in SLE patients. Atherosclerosis. 2012;225:224-230. https://doi.org/10.1016/j.atherosclerosis.2012.08.029

Volkmann ER, Grossman JM, Sahakian LJ, et al. Low physical activity is associated with proinflammatory high-density lipoprotein and increased subclinical atherosclerosis in women with systemic lupus erythematosus. Arthritis Care Res. 2010;62:258-265. https://doi.org/10.1002/acr.20076

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;43:54-65. DOI: https://doi.org/10.3899/jrheum.150460.

Parodis B, Sjowall C, Jonsen A, et al. Smoking and pre-existing organ damage reduce the efficacy of belimumab in systemic lupus erythematosus. Autoimmun. Rev. 2017;16: 343-351. https://doi.org/10.1016/j.autrev.2017.02.005

Bonciani D, Antiga E, Bonciolini V, et al. Homocysteine serum levels are increased and correlate with disease severity in patients with lupus erythematosus, Clin. Exp. Rheumatol. 34 (2016) 76e81. DOI:10.1007/s100670200115

Rho YH, Solus J, Raggi P, et al. Macrophage activation and coronary atherosclerosis in systemic lupus erythematosus and rheumatoid arthritis. Arthritis Care Res. 2011;63: 535-541. https://doi.org/10.1002/acr.20365

Lertratanakul A, Wu P, Dyer AR, et al. Risk factors in the progression of subclinical atherosclerosis in women with systemic lupus erythematosus. Arthritis Care Res. 2014;66:1177-1185. https://doi.org/10.1002/acr.22271.

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;37:322-329.  DOI: https://doi.org/10.3899/jrheum.090306

Huang YL, Chung HT, Chang CJ, Yeh KW, Chen LC, Huang JL. Lymphopenia is a risk factor in the progression of carotid intima-media thickness in juvenile-onset systemic lupus erythematosus. Arthritis Rheum. 2009;60: 3766-3775. https://doi.org/10.1002/art.25019

Gustafsson JT, Herlitz Lindberg M, Gunnarsson I, et al. Excess atherosclerosis in systemic lupus erythematosus,-A matter of renal involvement: case control study of 281 SLE patients and 281 individually matched population controls. PloS One. 2017;12: e0174572. https://doi.org/10.1371/journal.pone.0174572

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;43:745-750. DOI: https://doi.org/10.3899/jrheum.150437

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;20:1260-1266. https://doi.org/10.1177%2F0961203311411347

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;R155. https://doi.org/10.1186/ar3895

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;71:408-414 doi: 10.1136/annrheumdis-2011-200071

Leonard D, Svenungsson E, Dahlqvist J, et al. Novel gene variants associated with cardiovascular disease in systemic lupus erythematosus and rheumatoid arthritis. Ann Rheum Dis. 2018; pii: annrheumdis-2017-212614. doi: 10.1136/annrheumdis-2017-212614

Blazer A, Wang B, Simpson D, et al. Apolipoprotein L1 risk variants associate with prevalent atherosclerotic disease in African American systemic lupus erythematosus patients. PLoS One. 2017; 12:e0182483. doi: 10.1371/journal.pone.0182483

Tyden 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:e000508 doi: 10.1136/rmdopen-2017-000508

Buie JJ, Renaud LL, Muise-Helmericks R, Oates JC. IFN-alpha negatively regulates the expression of endothelial nitric oxide synthase and nitric oxide production: implications for systemic lupus erythematosus. J Immunol 2017; 199:1979–1988.  doi: 10.4049/jimmunol.1600108

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;34:617-623. https://doi.org/10.1007/s00296-013-2875-0

Smith CK, Vivekanandan-Giri A, Tang C, et al. Neutrophil extracellular trap-derived enzymes oxidize high-density lipoprotein: an additional proatherogenic mechanism in systemic lupus erythematosus, Arthritis Rheumatol. (Hoboken, NJ). 2014;66: 2532-2544. https://doi.org/10.1002/art.38703

Batuca JR, Ames PR, Amaral M, Favas C, Isenberg DA, Delgado J. Anti-atherogenic and anti-inflammatory properties of high-density lipoprotein are affected by specific antibodies in systemic lupus erythematosus. Rheumatol. Oxf. Engl. 2009;48:26-31. https://doi.org/10.1093/rheumatology/ken397

Clement M, Charles N, Escoubet B, et al. CD4flCXCR3fl T cells and plasmacytoid dendritic cells drive accelerated atherosclerosis associated with systemic lupus erythematosus. J Autoimmun. 2015; 63:59–67. doi: 10.1155/2016/5045248

Wilhelm AJ, Rhoads JP, Wade NS, Major AS. Dysregulated CD4fl T cells from SLE-susceptible mice are sufficient to accelerate atherosclerosis in LDLr-/- mice. Ann Rheum Dis. 2015; 74:778–785. doi:10.1136/annrheumdis-2013-203759

Li J, McArdle S, Gholami A, et al. CCR5flT-betflFoxP3fl effector CD4 T cells drive atherosclerosis. Circ Res. 2016; 118:1540–1552. doi: 10.1161/CIRCRESAHA.116.308648

Smith E, Croca S, Waddington KE, et al. Cross-talk between iNKT cells and monocytes triggers an atheroprotective immune response in SLE patients with asymptomatic plaque. Sci Immunol. 2016; 1: pii: eaah4081. doi: 10.1126/sciimmunol.aah4081

Margutti P, Matarrese P, Conti F, et al. Autoantibodies to the C-terminal subunit of RLIP76 induce oxidative stress and endothelial cell apoptosis in immune-mediated vascular diseases and atherosclerosis. Blood. 2008;111: 4559-4570. doi: https://doi.org/10.1182/blood-2007-05-092825

Farzaneh-Far MJ, Roman MD, Lockshin RB, et al. Relationship of antiphospholipid antibodies to cardiovascular manifestations of systemic lupus erythematosus. Arthritis Rheum. 2006;54:3918-3925. https://doi.org/10.1002/art.22265

Conti F, Spinelli FR, Alessandri C, et al. Subclinical atherosclerosis in systemic lupus erythematosus and antiphospholipid syndrome: focus on beta2GPI-specific T cell response. Arterioscler Thromb Vasc Biol. 2014; 34:661–668. doi: 10.1161/ATVBAHA

Zhang X, Xie Y, Zhou H, et al. Involvement of TLR4 in oxidized LDL/beta2GPI/antibeta2GPI-induced transformation of macrophages to foam cells. J Atheroscler Thromb. 2014; 21:1140–1151.

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; 56:3759–3769. DOI:10.1002/art.23035

Li J, Fu Q, Cui H, et al. Interferon-alpha priming promotes lipid uptake and macrophage-derived foam cell formation: a novel link between interferon-alpha and atherosclerosis in lupus. Arthritis Rheum. 2011;63:492-502. https://doi.org/10.1002/art.30165

Ghazarian M, Revelo XS, Nohr MK, et al. Type I interferon responses drive intrahepatic T cells to promote metabolic syndrome. Sci Immunol. 2017; 2: pii: eaai7616. doi: 10.1126/sciimmunol.aai7616.

King KR, Aguirre AD, Ye YX, et al. IRF3 and type I interferons fuel a fatal response to myocardial infarction. Nat Med. 2017; 23:1481–1487 doi: 10.1038/nm.4428

Mozzini C, Garbin U, Fratta Pasini AM, Cominacini L. An exploratory look at NETosis in atherosclerosis. Intern. Emerg. Med. 2017;12: 13-22. doi: 10.1007/s11739-016-1543-2.

Pieterse E, Rother N, Garsen M, et al. Neutrophil extracellular traps drive endothelial-to-mesenchymal transition. Arterioscler Thromb Vasc Biol. 2017; 37:1371–1379. doi: 10.1161/ ATVBAHA.117.309002. 

Westerweel PE, Luijten RK, Hoefer IE, Koomans HA, Derksen RH, Verhaar MC. Haematopoietic and endothelial progenitor cells are deficient in quiescent systemic lupus erythematosus. Ann. Rheum. Dis.2007; 66: 865-870. http://dx.doi.org/10.1136/ard.2006.065631,

Reynolds J, Ray D, Alexander MY, Bruce I. Role of vitamin D in endothelial function and endothelial repair in clinically stable systemic lupus erythematosus. Lancet (Lond. Engl.) 2015;385 (Suppl 1): S83. doi: 10.1016/S0140-6736(15)60398-1

Castejon R, Jimenez-Ortiz C, Valero-Gonzalez S, Rosado S, Mellor S, Yebra-Bango M. Decreased circulating endothelial progenitor cells as an early risk factor of subclinical atherosclerosis in systemic lupus erythematosus, Rheumatol. Oxf. Engl. 2014;53: 631-638. https://doi.org/10.1093/rheumatology/ket367

Svenungsson E, Engelbertsen D, Wigren M, et al. Decreased levels of autoantibodies against apolipoprotein B-100 antigens are associated with cardiovascular disease in systemic lupus erythematosus. Clin. Exp. Immunol. 2015;181:417-426. https://doi.org/10.1111/cei.12651

Gronwall C, Reynolds H, Kim J.K, et al. Relation of carotid plaque with natural IgM antibodies in patients with systemic lupus erythematosus, Clin. Immunol. Orl. Fla. 2014;153:1e7. https://doi.org/10.1016/j.clim.2014.03.017

Zhang L, Fu T, Yin R, Zhang Q, Shen B. Prevalence of depression and anxiety in systemic lupus erythematosus: a systematic review and metaanalysis. BMC Psychiatry 2017;17: 70. https://doi.org/10.1016/j.matlet.2017.01.132

Moraleda V, Prados G, Martinez MP, Sanchez AI, Sabio JM, Miro E. Sleep quality, clinical and psychological manifestations in women with systemic lupus erythematosus, Int. J. Rheum. Dis. 2017; 19. http://dx.doi.org/ 10.1111/1756-185X.13081.

Jorge A, Lertratanakul J, Lee W, et al. Depression and progression of subclinical cardiovascular disease in systemic lupus erythematosus. Arthritis Care Res. 2017;69: 5-11. https://doi.org/10.1002/acr.22992

Juarez-Rojas JG, Medina-Urrutia AX, Jorge-Galarza E, et al. Pioglitazone improves the cardiovascular profile in patients with uncomplicated systemic lupus erythematosus: a double-blind randomized clinical trial. Lupus 2012;21:27-35. https://doi.org/10.1177%2F0961203311422096

Duran-Barragan S, McGwin Jr G, Vila LM, Reveille JD, Alarcon GS. Angiotensin-converting enzyme inhibitors delay the occurrence of renal involvement and are associated with a decreased risk of disease activity in patients with systemic lupus erythematosuseresults from LUMINA (LIX): a multiethnic US cohort. Rheumatol. Oxf. Engl. 2008;47:1093-1096. https://doi.org/10.1093/rheumatology/ken208

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. 2011;63:875-883. https://doi.org/10.1002/acr.20440

Schanberg LE, Sandborg C, Barnhart HX, et al. Use of atorvastatin in systemic lupus erythematosus in children and adolescents. Arthritis Rheum. 2012;64:285-296. https://doi.org/10.1002/art.30645

Petri MA, Kiani AN, Post W, Christopher-Stine L, Magder LS. Lupus atherosclerosis prevention study (LAPS). Ann. Rheum. Dis. 2011;70:760-765. http://dx.doi.org/10.1136/ard.2010.136762

Woo JM, Lin Z, Navab M, et al. Treatment with apolipoprotein A-1 mimetic peptide reduces lupus-like manifestations in a murine lupus model of accelerated atherosclerosis. Arthritis Res. Ther. 2012;12:R93. https://doi.org/10.1186/ar3020

Ponticelli C, Moroni G. Hydroxychloroquine in systemic lupus erythematosus (SLE). Expert Opin Drug Saf. 2017; 16:411–419. doi: 10.1080/14740338.2017

Ruiz-Arruza I, Lozano J, Cabezas-Rodriguez I, et al. Restrictive use of oral glucocorticoids in systemic lupus erythematosus and prevention of damage without worsening long-term disease control: an observational study. Arthritis Care Res (Hoboken). 2018; 70:582–591. doi: 10.1002/acr.23322

Furumoto Y, Smith CK, Blanco L, et al. Tofacitinib ameliorates murine lupus and its associated vascular dysfunction. Arthritis Rheumatol. 2017; 69:148–160. doi: 10.1002/art.39818.

Huo Y, Li J, Qin X, et al. Efficacy of folic acid therapy in primary prevention of stroke among adults with hypertension in China: the CSPPT randomized clinical trial. Jama. 2015;313:1325-1335. doi:10.1001/jama.2015.2274




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