Skip to main content

Advertisement

Log in

Dyslipidemia in systemic lupus erythematosus

  • Novel Aspects in Lupus, 2017
  • Published:
Immunologic Research Aims and scope Submit manuscript

Abstract

Cardiovascular disease is one of the major causes of morbidity and mortality in patients with systemic lupus erythematosus (SLE). Accelerated atherosclerosis is related to traditional (age, hypertension, diabetes mellitus, dyslipidemia, obesity, smoking, and positive family history) and non-traditional, disease-related factors. Traditional risk factors are still more prominent in patients with lupus, as both hypertension and hypercholesterinemia were independently associated with premature atherosclerosis in several SLE cohorts. In this work, the authors summarize the epidemiology of dyslipidemia in lupus patients and review the latest results in the pathogenesis of lipid abnormalities. The prevalence of dyslipidemia, with elevations in total cholesterol (TC), low-density lipoprotein (LDL), triglyceride (TG), and apolipoprotein B (ApoB), and a reduction in low-density lipoprotein (LDL) levels are about 30% at the diagnosis of SLE rising to 60% after 3 years. Multiple pathogenetic mechanism is included, C-reactive protein (CRP) and erythrocyte sedimentation rate (ESR) can suppress HDL and increase TG, auto-antibodies can cause the injury of the endothelium, lipoprotein lipase (LPL) activity can be reduced by circulating inflammatory mediators and antibodies, and increased oxidative stress may trigger a wide range of pro-atherogenic lipid modifications. As a major risk factor, dyslipidemia should be treated aggressively to minimize the risk of atherosclerosis and cardiovascular events. Randomized controlled trials with statins are controversial in the detention of atherosclerosis progression, but can be favorable by inhibiting immune activation that is the arterial wall and by decreasing lupus activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Abbreviations

anti-oxLDL:

Anti oxidized low-density lipoprotein

Apo:

Apolipoprotein

β2GPI β2 :

glikoproteini

CEC:

Cholesterol efflux capacity

cIMT:

Carotid intima-media thickness

CRP:

C-reactive protein

CV:

Cardiovascular

CVD:

Cardiovascular disease

DNA:

Deoxyribonucleic acid

ED:

Endothel dysfunction

ESR:

Erythrocyte sedimentation rate

HCQ:

Hydroxychloroquine

HDL:

High-density lipoprotein

IDL:

Intermediate-density lipoprotein

IFN-γ:

Interferon γ

ICAM:

Intracellular cell adhesion molecule

Ig:

Immunoglobulin

IL:

Interleukin

LDL:

Low-density lipoprotein

LPL:

Lipoprotein lipase

LN:

Lupus nephritis

MCP-1:

Monocyte chemoattractant protein-1

MPO:

Myeloperoxidase

NET:

Neutrophil extracellular trap

NOS:

Nitric oxide synthetase

NOX:

NADPH oxidase

oxLDL:

Oxidized low-density lipoprotein

PAF-AH:

Platelet activating factor acetylhydrolase

PON:

Paraoxonase

SSA:

Serum amyloid A

SLAM-R:

Systemic lupus activity measure-revised

SLE:

Systemic lupus erythematosus

SLEDAI:

Systemic lupus erythematosus disease activity

TC:

Total cholesterol

TG:

Triglyceride

TNF-α:

Tumor necrosis factor α

VCAM:

Vascular cell adhesion molecule

VEGF:

Vascular endothelial growth factor

VLDL:

Very low-density lipoprotein

References

  1. Yukovich M, Vostretsova K, Chen W, Avina-Zubieta JA. Overall and cause-specific mortality in pateints with systemic lupus erythematosus: a meta-analysis of observational studies. Arthritis Care Res (Hoboken). 2014;66:608–16.

    Article  Google Scholar 

  2. Hollan I, Meroni PL, Ahearn JM, Cohen Tervaert JW, Curran S, Goodyear CS, et al. Cardiovascular disease in autoimmune rheumatic diseases. Autoimm Rev. 2013;12:1004–15.

    Article  CAS  Google Scholar 

  3. Esdaile JM, Abrahamowicz M, Grodzicky T, Li Y. Panaritis C, du Berger R et al. Traditional Framingham risk factors failed to fully account for accelerated atherosclerosis in systemic lupus erythematosus. 2001;44(10):2331–7.

    CAS  Google Scholar 

  4. Urowitz MB, Ibanez D, Gladmann DD. Adjusted Framingham risk factor scoring for systemic lupus erythematosus. Arthritis Reum 2011:1 (ACR Meeting abstracts, abstract number: 647)

  5. Symmons DP, Gabriel SE. Epidemiology of CVD in rheumatic disease, with a focus on RA and SLE. Nat Rev Rheumatol. 2011;7(7):399–408.

    Article  PubMed  Google Scholar 

  6. Cervera R, Khamashta MA. Epidemiology of systemic lupus erythematosus at the change of the millenium: lessons from the euro-lupus and the LUMINA projects. Lupus. 2006;15(1):1–2.

    Article  PubMed  Google Scholar 

  7. Manzi S, Meilahn EN, Rairie JE, Conte CG, Medsger Jr TA, Jansen-McWilliams L, et al. Ag-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus: comparison with the Framingham study. Am J Epidemiol. 1997;145:408–5.

    Article  CAS  PubMed  Google Scholar 

  8. Urowitz MB, Gladman D, Ibañez D, Sanchez-Guerrero J, Bae S, Clarke A, et al. Clinical manifestations and coronary artery disease risk factors at diagnosis of systemic lupus erythematosus: data from an international inception cohort. Lupus. 2007;16(9):731–5.

    Article  CAS  PubMed  Google Scholar 

  9. Urowitz MB, Gladmann DD, Ibanez D, Fortin P, Sanchez-Guerrero J, Bae A, et al. Accumulation of coronary artery disease risk factors over three years: data from an inernational inception cohort. Arthritis Rheum. 2008;59:176–80.

    Article  CAS  PubMed  Google Scholar 

  10. Bruce IN, Urowitz MB, Gladmann DD, Hallett DC. The natural history of hypercholesterinemia in SLE. J Rheumatol. 1999;26:2137–43.

    CAS  PubMed  Google Scholar 

  11. Borba EF, Bonfa E. Dyslipoproteinemias in systemic lupus erythematosus: influence of disease, activity, and anticardiolipin antibodies. Lupus. 1997;6(6):533–9.

    Article  CAS  PubMed  Google Scholar 

  12. Iowite NT, Samuel P, Ginzler E, Jacobson MS. Dyslipoproteinemia in pediatric systemic lupus erythematosus. Arthritis Rheum. 1988;31:859–63.

    Article  Google Scholar 

  13. Soep JB, Mietus-Snyder M, Malloy MJ, Witzum JL, von Scheven E. Assessment of atherosclerotic risk factors and endothelial function in children and young adults with pediatric-onset systemic lupus erythematosus. Arthritis Rheum. 2004;51(3):451–7.

    Article  PubMed  Google Scholar 

  14. Ardoin SP, Schanberg LE, Sandborg C, Yow E, Barnhart HX, Mieszkalski KI. Laboratory markers of cardiovascular risk in pediatric SLE: the APPLE baseline cohort. Lupus. 2010;19(11):1315–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Posadas-Romero C, Torres-Tamayo M, Zamora-Gonzalez J, Aguilar-Herrera BE, Posadas-Sanchez R, Cardoso-Saldana G, et al. High insulin levels and increased low-density lipoprotein oxidizability in pediatric pateints with systemic lupus erythematosus. Arthritis & Rheum. 2004;50(1):160–5.

    Article  CAS  Google Scholar 

  16. Maroz N. Segal MS: lupus nephritis and end-stage kidney disease. Am J Med Sci. 2013;346(4):319–23.

    Article  PubMed  Google Scholar 

  17. Liu L, Zhang T, Ye Y, Zhang S, Chen L. Analysis of traditional cardiovascular risk factors in patients with systemic lupus erythematosus. Zhonghua Xin Xue Guan Bing Za Zhi. 2014;42(9):753–8.

    PubMed  Google Scholar 

  18. Chong YB, Yap DY, Tang CS, Chan TM. Dislipidemia in patients with lupus nephritis. Nephrology (Carlton). 2011;16(5):511–7.

    Article  Google Scholar 

  19. Luzar B, Ferluga D. Role of lipids in the progression of renal disease in systemic lupus erythematosus patients. Wien Klin Wochenschr. 2000;112:716–21.

    CAS  PubMed  Google Scholar 

  20. Brown WV. Lipoprotein disorders in diabetes mellitus. Med Clin North Am. 1994;78:143–61.

    Article  CAS  PubMed  Google Scholar 

  21. Bhakte SK, Sarker A. Effect of serum lipoprotein (a) [Lp(a)] in menopausal women. Mymensingh Med J. 2016;25(2):255–60.

    Google Scholar 

  22. Narshi CB, Giles IP, Rahman A. The endothelium: an interface between autoimmunity and atherosclerosis in systemic lupus erythematosus? Lupus. 2011;20(1):5–13.

    Article  CAS  PubMed  Google Scholar 

  23. Ronda N, Favari E, Borghi MO, Ingegnoli F, Gerosa M, Chighizola C, et al. Impaired serum cholesterol efflux capacity in rheumatoid arthritis and systemic lupus erythematosus. Ann Rheum Dis. 2014;73(3):609–15.

    Article  PubMed  Google Scholar 

  24. Ginsberg HN. Lipoprotein physiology. Endocrinol Metab Clin N Am. 1998;27(3):503–19.

    Article  CAS  Google Scholar 

  25. Borba E, Bonfa E, Vinagre CGC, Ramires JAF, Maranhao RC. Chylomicron metabolism is markedly altered in systemic lupus erythematosus. Arthritis Rheum. 2000;43(5):1033–40.

    Article  CAS  PubMed  Google Scholar 

  26. Cooper AD. Hepatic uptake of chylomicron remnants. J Lipid Res. 1994;38(11):2173–92.

    Google Scholar 

  27. De Carvalho JF, Bonfa E, Borba EF. Systemic lupus erythematosus and lupus dyslipoproteinemia. Autoimmun Rev. 2008;7:246–50.

    Article  PubMed  Google Scholar 

  28. De Carvalho JF, Borba EF, Viana VS, Bueno C, Leon EP, Bonfa E. Antilipoprotein lipase antibodies: a new plyayer in the complex atherosclerotic process in systemic lupus erythematosus? Arthritis Rheum. 2004;50:3610–5.

    Article  CAS  PubMed  Google Scholar 

  29. Reichlin M, Fesmire J. Quintero-del-Rio Al, Wolfson–Reichlin M. Autoantibodies to lipoprotein lipase and dyslipidemia in systemic lupus erythematosus. Arthritis Rheum. 2002;46:2957–63.

    Article  CAS  PubMed  Google Scholar 

  30. Song LJ, Liu WW, Fan YC, Qui F, Chen QL, Li XF, et al. The positive correlations of apolipoprotein E with disease activity and related cytokines in systemic lupus erythematosus. Diagn Pathol. 2013;8:175.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Lahita RG, Rivkin E, Cavanagh I, Romano P. Low levels of total cholesterol high-density lipoprotein and apolipoprotein A1 in association with anticardiolipin antibodies in patients with systemic lupus erythematosus. Arthritis Rheum. 1993;36:1566–74.

    Article  CAS  PubMed  Google Scholar 

  32. Svenungsson E, Engelbertsen D, Wigren M, Gustafsson JT, Gunarsson I, Elvin K, et al. Decreased levels of autoantibodies against apolipoprotein B-100 antigens are associated with cardiovascular disease in systemic lupus erythematosus. Clin Exp Immunol. 2015;181:417–26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Borba EF, Carvalho JF, Bonfa E. Mechanisms of dyslipoproteinemias in systemic lupus erythematosus. Clin Dev Immunol. 2006;13(2–4):203–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Frostegard J, Svenungsson E, Wu R, Gunarsson I, Lundberg IE, Klareskog L, et al. Lipid peroxidation is enhanced in patients with systemic lupus erythematosus and is associated with arterial and renal manifestations. Arthritis Rheum. 2005;52:192–200.

    Article  CAS  PubMed  Google Scholar 

  35. Navab M, Ananthramaiah GM, Reddy ST, Van Lenten BJ, Ansell BJ, Fonarow GC, et al. The oxidation hypothesis of atherogenesis: the role of oxidized phospholipids and HDL. J Lipid Res. 2004;45:993–1007.

    Article  CAS  PubMed  Google Scholar 

  36. Parthasarathy S, Barnett J, Fong LG. High-density lipoprotein inhibits the oxidative modification of low-density lipoprotein. Biochim Biophys Acta. 1990;1044:275–83.

    Article  CAS  PubMed  Google Scholar 

  37. Smith CK, Vuvekanandan-Giri A, Tang C, Knight JS, Mathew A, Padilla RL, et al. Neutrophil extracellular trap-derived enzymes oxidize high-density lipoprotein: an additional proatherogenic mechanism in systemic lupus erythematosus. Arthritis Rheumatol. 2014;66(9):2532–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Van Lenten BJ, Hama SY, De Beer FC, Stafforini DM, McIntyre TM, Prescott SM, et al. Anti-inflammatory HDL becomes pro-inflammatory during the acute phase response. Loss of protective effect of HDL against LDL oxidation in aortic wall cell co-cultures. J Clin Invest. 1995;96:2758–67.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Parra SM, Vives G, Ferré R, González M, Guardiola M, Ribalta J, et al. Complement system and small HDL particles are associated with subclinical atherosclerosis in SLE patients. Atherosclerosis. 2012;225:224–30.

    Article  CAS  PubMed  Google Scholar 

  40. Kowalska K, Socha E, Milnerowicz H. Review: the role of paraoxonase in cardiovascular diseases. Ann Clin Lab Sci. 2015;45(2):226–33.

    CAS  PubMed  Google Scholar 

  41. Gaál K, Tarr T, Lőrinc H, Borbás V, Seres I, Harangi M, et al. High-density lipoprotein antioxidant capacity, subpopulation distribution and paraoxonase-1 activity in patients with systemic lupus erythematosus. Lipids Health Dis. 2016;15:60.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Kiss E, Seres I, Tarr T, Kocsis Z, Szegedi GY, Paragh G. Reduced paraoxonase1 activity is a risk for atherosclerosis in patients with systemic lupus erythematosus. Ann N Y Acad Sci. 2007;1108:83–91.

    Article  CAS  PubMed  Google Scholar 

  43. Tripi LM, Manzi S, Chen Q, Kenney M, Shaw P, Kao A. Relationship of serum paraoxonase 1 activity and paraoxonase 1 genotype to risk of systemic lupus erythematosus. Arthritis Rheum. 2006;54(6):1928–39.

    Article  CAS  PubMed  Google Scholar 

  44. Dasgupta S, Demirci FY, Dressen AS, Kao AH, Rhew EZ, Ramsey-Goldman R. Association analysis of PON2 genetic variants with serum paraoxonase activity and systemic lupus erythematosus. BMC Med Genet. 2011;12:7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Vaarla O, Alfthan G, Jauhiainen M, Leirisalo-Repo M, Aho K, Palosuo T. Cross-reaction between antibodies to oxidized low-density lipoprotein and to cardiolipin in systemic lupus erythematosus. Lancet. 1993;341:923–5.

    Article  Google Scholar 

  46. Delgado Alves J, Kumar S, Isenberg DA. Cross-reactivity between anti-cardiolipin, anti-high-density lipoprotein and anti-apoliprotein A1 IgG antibodies in patients with systemic lupus erythematosus and primary antiphospholid syndrome. Rheumatology. 2003;42:893–9.

    Article  CAS  PubMed  Google Scholar 

  47. Lopez LR, Simpson DF, Hurley BL, Matsuura E. OxLDL/beta2GPI complexes and autoantibodies in patients with systemic lupus erythematosus, systemic sclerosis and antiphospholipid syndrome: pathogenic implications for vascular involvment. Ann N Y Acad Sci. 2005;1051:313–22.

    Article  CAS  PubMed  Google Scholar 

  48. Lopez LR, Salazar-Paramo M, Palafox-Sanchez C, et al. Oxidized low-density lipoprotein and beta2-glycoprotein I in patients with systemic lupus erythematosus and increased carotid intima-media thickness: implications in autoimmune-mediated atherosclerosis. Lupus. 2006;15(2):80–6.

    Article  CAS  PubMed  Google Scholar 

  49. Maury CPJ, Teppo AM. Tumor necrosis factor in the serum of patients with systemic lupus erythematosus. Arthritis Rheum. 1989;32:146–50.

    Article  CAS  PubMed  Google Scholar 

  50. Svenungsson E, Fei GZ, Jensen-Urstad K, et al. TNF-alpha: a link between hypertriglyceridaemia and inflammation in SLE patients with cardiovascular disease. Lupus. 2003a;12(6):454–61.

    Article  CAS  PubMed  Google Scholar 

  51. Beutler B, Mahoney J, Le Trang N, et al. Purification of cachectin, a lipoprotein lipase-suppressing hormone secreted by endotoxin-induced RAW 264.7 cells. J Exp Med. 1985;161:984–95.

    Article  CAS  PubMed  Google Scholar 

  52. Feinberg B, Kurzrock R, Talpaz M, Blick M, Saks S, Gutterman JU. A phase I trial of intravenously-administered recombinant tumor necrosis factor-alpha in cancer patients. J Clin Oncol. 1988;6:1328–34.

    Article  CAS  PubMed  Google Scholar 

  53. Gombos T, Förhécz Z, Pozsonyi Z, Jánoskuti L, Prohászka Z, Karádi I. Long-term survival and apolipoprotein A1 level in chronic heart failure: interaction with the TNFa-308 G/a polymorphism. J Card Fail. 2016;S1071-9164(16):30107–5.

    Google Scholar 

  54. Hyka N, Dayer JM, Modoux C, Kohno T, CKCK 3rd E, Roux-Lombard P, et al. Apolipoprotein A-I inhibits the production of interleukin-1 and tumor necrosis factor by blocking contact-mediated activation of monocytes by T lymphocytes. Blood. 2001;97:2381–9.

    Article  CAS  PubMed  Google Scholar 

  55. Tölle M, Huang T, Schuchardt M, Jankowski V, Prüfer N, Jankowski J, et al. High-density lipoprotein loses its anti-inflammatory capacity by accumulation of pro-inflammatory –serum amyloid a. Cardiovasc Res. 2012;94:154–62.

    Article  PubMed  Google Scholar 

  56. 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.

    CAS  PubMed  Google Scholar 

  57. Ettinger WH, Goldberg AP, Applebaum-Bowden D, Hazzard WR. Dyslipoproteinemia in systemic lupus erythematosus. Effects of corticosteroids Am J Med. 1987;83:503–8.

    CAS  PubMed  Google Scholar 

  58. Petri M, Lakata C, Magder L, Goldman D. Effect of prednisone and hydroxychloroquine on coronary artery disease risk factors in systemic lupus erythematosus: a longitudinal data analysis. Am J Med. 1994;96:254–9.

    Article  CAS  PubMed  Google Scholar 

  59. Arnaldi G, Scandali VM, Trementino L, Cardialetti M, Appolloni G, Boscaro M. Pathophysiology of dyslipidaemia in Cushing’s syndrome. Neuroendocrinology. 2010;92:86–90.

    Article  CAS  PubMed  Google Scholar 

  60. Hussain AA, Bruce IN. Risk facors for coronary heart disease in connective tissue diseases. Ther Adv Muskulosclet Dis. 2010;2(3):145–53.

    Article  Google Scholar 

  61. Germano V, Picchianti Diamanti A, Ferlito C, Podestra E, Salemi S, Migliore A, et al. Cyclosporine a in the long term management of systemic lupus erythematosus. J Biol Regul Homeost Agents. 2011;25:397–403.

    CAS  PubMed  Google Scholar 

  62. Cairoli E, Rebella M, Danese N, Garra V, Borba EF. Hydroxychloroquine reduces low-density lipoprotein cholesterol levels in systemic lupus erythematosus: a longitudinal evaluation of the lipid-lowering effect. Lupus. 2012;21:1178–82.

    Article  CAS  PubMed  Google Scholar 

  63. Tam LS, Li EK, Lam CW, Tomlinson B. Hydroxychloroquine has no significant effect on lipids and apolipoproteins in Chinese systemic lupus erythematosus patients with mild or inactive disease. Lupus. 2000;9(6):413–6.

    Article  CAS  PubMed  Google Scholar 

  64. Fernández-Nebro A, Marenco JL, López-Longo F, Galindo M, Hernández-Cruz BE, Narváez J, et al. The effects of rituximab on the lipid profile of patients with active systemic lupus erythematosus: results from a nationwide cohort in Spain (LESIMAB). Lupus. 2014;23(10):01014–22.

    Article  Google Scholar 

  65. Schanberg LE, Sandborg C, Barnhart HX, Ardoin SP, Yow E, Evans GW, et al. Use of atorvastatin in systemic lupus erythematosus in children and adolescents. Arthritis Rheum. 2012;64:285–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Petri MA, Kiani AN, Post W, Christopher-Stine L, Magder LS. Lupus atherosclerosis prevention study (LAPS). Ann Rheum Dis. 2011;70:760–5.

    Article  CAS  PubMed  Google Scholar 

  67. Abud-Mendoza C, de la Fuente H, Cuevas-Orta E, Baranda L, Cruz-Rio J, González-Amaro R. Therapy with statins in patients with refractory rheumatic diseases: a preliminary study. Lupus. 2003;12:607–11.

    Article  CAS  PubMed  Google Scholar 

  68. Ferreira GA, Navarro TP, Telles RW, Andrade LE, Sato EI. Atorvastatin therapy improves endothelial-dependent vasodilatation in patients with systemic lupus erythematosus: an 8 weeks controlled trial. Rheumatology (Oxford). 2007;46:1560–5.

    Article  CAS  Google Scholar 

  69. De Kruif MD, Limper M, Hansen HR, De Ruiter J, Spek CA, Van Gorp EC, et al. Effects of a 3-months course of rosuvastatin in patients with systemic lupus erythematosus. Ann Rheum Dis. 2009;68:1654.

    Article  CAS  PubMed  Google Scholar 

  70. 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;63:875–83.

    Article  CAS  Google Scholar 

  71. Costenbader KH, Liang MH, Chibnik LB, Aizer J, Kwon H, Gall V, et al. A pravastatin dose-escalation study in systemic lupus erythematosus. Rheumatol Int. 2007;27:1071–7.

    Article  CAS  PubMed  Google Scholar 

  72. Norby GE, Holme I, Fellstrom B, Jardine A, Cole E, Abedini S, et al. Effect of fluvastatin on cardiac outcomes in kidney transplant patients with systemic lupus erythematosus: a randomized placebo-controlled study. Arthritis Rheum. 2009;60:1060–4.

    Article  CAS  PubMed  Google Scholar 

  73. Costenbader KH, Karlson EW, Gall V, De Pablo P, Finkch A, Lynch M, et al. Barriers to a trial of atherosclerosis prevention in systemic lupus erythematosus. Arthritis Rheum. 2005;53:718–23.

    Article  PubMed  Google Scholar 

  74. Tselios K, Koumaras C, Gladman DD, Urowitz MB. Dyslipidemia in systemic lupus erythematosus: just another comorbidity? Semin Arthritis Rheum. 2016;45(5):604–10.

    Article  CAS  PubMed  Google Scholar 

  75. Rosen AB, Tsai JS, Downs SM. Variations in risk attitude across race, gender, and education. Med Decis Mak. 2003;23:511–7.

    Article  Google Scholar 

  76. Vera-Lastra O, Méndez-Flores S, Cruz-Dominguez MP, Medina G, Calderón-Aranda E, Jara LJ. Effect of ezetimibe plus pravastatin on endothelial dysfunction in patients with systemic lupus erythematosus. Lupus. 2016.

  77. Willis R, Self AM, McGwin Jr GG, Martinez-Martinez LA, Gonzalez EB, Doan E, et al. Effects of statins on proinflammatory/prothrombotic biomarkers and multi-ethnic US cohort. Clin Exp Rheumatol. 2014;32:162–7.

    CAS  PubMed  Google Scholar 

  78. Soubrier M, Mathieu S, Hermet M, Makarawiecz C, Bruckert E. Do all lupus patients need statins? Join Bone Spine. 2013;80:244–9.

    Article  Google Scholar 

  79. Van Leuven SI, Mendez-Fernandez YV, Stroes ES, Tak PP, Major AS. Statin therapy in lupus-mediated atherogenesis: two birds with one-stone? Ann Rheum Dis. 2011;70:245–8.

    Article  CAS  PubMed  Google Scholar 

  80. Greenwood J, Steinman L, Zamvil SS. Statin therapy and autoimmune disease: from proetin prenylation to immunomodulation. Nat Rev Immunol. 2006;6:358–70.

    Article  CAS  PubMed  Google Scholar 

  81. Noel B. Lupus erythematosus and other autoimmune diseases related to statin therapy: a systematic review. J Eur Aca Dermatol Venerol. 2007;21(1):17–24.

    Article  CAS  Google Scholar 

  82. Moulis G, Béné J, Sommet A, Sailur L, Lapeyre-Mestre M, Montastruc JL, et al. Statin-induced lupus: a case/non-case study in a nationwide pharmacovigilance database. Lupus. 2012;21(8):885–9.

    Article  CAS  PubMed  Google Scholar 

  83. Voloshyna I, Teboul I, Littlefield MJ, Siegart NM, Turi GK, Fazzari MJ et al. Resveratrol counters systemic lupus erythematosus-associated atherogenicity by normalizing cholesterol efflux. Exp Biol Med (Maywood) 2016 Apr 27.

  84. Benatti FB, Miossi R, Passareli M, Nakandakare ER, Perandini L, Lima FR. The effects of exercise on lipid profile in systemic lupus erythematosus and healthy individuals: a randomized trial. Rheumatol Int. 2015;35(1):61–9.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Melinda Zsuzsanna Szabó.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Szabó, M.Z., Szodoray, P. & Kiss, E. Dyslipidemia in systemic lupus erythematosus. Immunol Res 65, 543–550 (2017). https://doi.org/10.1007/s12026-016-8892-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12026-016-8892-9

Keywords

Navigation