Prediction and management of cardiovascular outcomes in systemic lupus erythematosus

Expert Review of Clinical Immunology

Volumn 11, Issue 2, 2015, Pages 247-253

  Frostegard, Johan ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

antibodies; atherosclerosis; cardiovascular disease; inflammation; risk factors; systemic lupus erythematosus

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; PHOSPHOLIPID ANTIBODY; PHOSPHORYLCHOLINE;

ATHEROSCLEROTIC PLAQUE; CARDIOVASCULAR DISEASE; DIABETES MELLITUS; DISEASE ACTIVITY; DISEASE CONTROL; DYSLIPIDEMIA; HUMAN; HYPERTENSION; INFLAMMATION; NONHUMAN; OUTCOME ASSESSMENT; REVIEW; RISK FACTOR; SMOKING; SYSTEMIC LUPUS ERYTHEMATOSUS; ADVERSE EFFECTS; ATHEROSCLEROSIS; BLOOD; COMPLICATION; DIABETES COMPLICATIONS; DYSLIPIDEMIAS; LUPUS ERYTHEMATOSUS, SYSTEMIC;

ANTIBODIES, ANTIPHOSPHOLIPID; ATHEROSCLEROSIS; DIABETES COMPLICATIONS; DYSLIPIDEMIAS; HUMANS; HYPERTENSION; LUPUS ERYTHEMATOSUS, SYSTEMIC; RISK FACTORS; SMOKING;

EID: 84921367096     PISSN: 1744666X     EISSN: 17448409     Source Type: Journal    
DOI: 10.1586/1744666X.2015.993970     Document Type: Review

References (76)

1. Mayerl C, Lukasser M, Sedivy R, et al. Atherosclerosis research from past to present-on the track of two pathologists with opposing views, Carl von Rokitansky and Rudolf Virchow. Virchows Arch 2006; 449: 96-103
2. Tyrrell PN, Beyene J, Feldman BM, et al. Rheumatic disease and carotid intima-media thickness. a systematic review and meta-Analysis. Arterioscler Thromb Vasc Biol 2010; 30: 1014-26
3. Frostegard J. Immunity, atherosclerosis and cardiovascular disease. BMC Med 2013; 11: 117
4. Tabas I, Glass CK. Anti-inflammatory therapy in chronic disease: challenges and opportunities. Science 2013; 339: 166-72
5. Frostegard J, Ulfgren AK, Nyberg P, et al. Cytokine expression in advanced human atherosclerotic plaques: dominance of pro-inflammatory (Th1) and macrophage-stimulating cytokines. Atherosclerosis 1999; 145: 33-43
6. Xu Q, Dietrich H, Steiner HJ, et al. Induction of arteriosclerosis in normocholesterolemic rabbits by immunization with heat shock protein 65. Arterioscler Thromb 1992; 12: 789-99
7. Palinski W, Miller E, Witztum JL. Immunization of low density lipoprotein (LDL) receptor-deficient rabbits with homologous malondialdehyde-modified LDL reduces atherogenesis. Proc Natl Acad Sci USA 1995; 92: 821-5
8. Ait-Oufella H, Salomon BL, Potteaux S, et al. Natural regulatory T cells control the development of atherosclerosis in mice. Nat Med 2006; 12: 178-80
9. George J, Harats D, Gilburd B, et al. Adoptive transfer of beta(2)-glycoprotein I-reactive lymphocytes enhances early atherosclerosis in LDL receptor-deficient mice. Circulation 2000; 102: 1822-7
10. Zhou X, Robertson AK, Hjerpe C, Hansson GK. Adoptive transfer of CD4+ T cells reactive to modified low-density lipoprotein aggravates atherosclerosis. Arterioscler Thromb Vasc Biol 2006; 26: 864-70
11. Ewing MM, de Vries MR, Nordzell M, et al. Annexin A5 therapy attenuates vascular inflammation and remodeling and improves endothelial function in mice. Arterioscler Thromb Vasc Biol 2011; 31: 95-101
12. Cederholm A, Svenungsson E, Jensen-Urstad K, et al. Decreased binding of annexin v to endothelial cells: a potential mechanism in atherothrombosis of patients with systemic lupus erythematosus. Arterioscler Thromb Vasc Biol 2005; 25: 198-203
13. Liu A, Ming JY, Fiskesund R, et al. Induction of dendritic cell-mediated t-cell activation by modified but not native low-density lipoprotein in humans and inhibition by annexin A5: involvement of heat shock proteins. Arterioscler Thromb Vasc Biol 2014
14. Maganto-Garcia E, Tarrio M, Lichtman AH. Mouse models of atherosclerosis. Curr Protoc Immunol 2012; 15: 1-23
15. Matoba T, Sato K, Egashira K. Mouse models of plaque rupture. Curr Opin Lipidol 2013; 24: 419-25
16. Tupin E, Nicoletti A, Elhage R, et al. CD1d-dependent activation of NKT cells aggravates atherosclerosis. J Exp Med 2004; 199: 417-22
17. Cheng X, Yu X, Ding YJ, et al. The Th17/Treg imbalance in patients with acute coronary syndrome. Clin Immunol 2008; 127: 89-97
18. Li Q, Wang Y, Chen K, et al. The role of oxidized low-density lipoprotein in breaking peripheral Th17/Treg balance in patients with acute coronary syndrome. Biochem Biophys Res Commun 2010; 394: 836-42
19. Feig JE, Feig JL. Macrophages, dendritic cells, and regression of atherosclerosis. Front Physiol 2012; 3: 286
20. Liu P, Yu YR, Spencer JA, et al. CX3CR1 deficiency impairs dendritic cell accumulation in arterial intima and reduces atherosclerotic burden. Arterioscler Thromb Vasc Biol 2008; 28: 243-50
21. Millonig G, Niederegger H, Rabl W, et al. Network of vascular-Associated dendritic cells in intima of healthy young individuals. Arterioscler Thromb Vasc Biol 2001; 21: 503-8
22. Yilmaz A, Lochno M, Traeg F, et al. Emergence of dendritic cells in rupture-prone regions of vulnerable carotid plaques. Atherosclerosis 2004; 176: 101-10
23. Bobryshev YV, Watanabe T. Ultrastructural evidence for association of vascular dendritic cells with T-lymphocytes and with B-cells in human atherosclerosis. J Submicrosc Cytol Pathol 1997; 29: 209-21
24. Woollard KJ, Geissmann F. Monocytes in atherosclerosis: subsets and functions. Nat Rev Cardiol 2010; 7: 77-86
25. Leitinger N, Schulman IG. Phenotypic polarization of macrophages in atherosclerosis. Arterioscler Thromb Vasc Biol 2013; 33: 1120-6
26. Kovanen PT. Mast cells: multipotent local effector cells in atherothrombosis. Immunol Rev 2007; 217: 105-22
27. Willems S, Vink A, Bot I, et al. Mast cells in human carotid atherosclerotic plaques are associated with intraplaque microvessel density and the occurrence of future cardiovascular events. Eur Heart J 2013; 34(48): 3699-706
28. Agewall S, Eurenius L, Hofman-Bang C, et al. Myocardial infarction with angiographically normal coronary arteries. Atherosclerosis 2011; 219: 10-14
29. Su J, Frostegard AG, Hua X, et al. Low levels of antibodies against oxidized but not nonoxidized cardiolipin and phosphatidylserine are associated with atherosclerotic plaques in systemic lupus erythematosus. J Rheumatol 2013; 40: 1856-64
30. Bulkeley BH, Roberts WC. The Heart in Systemic Lupus Erythematosus and the changes Induced in it by Corticosteroid Therapy. Am J Med 1975; 58: 243-64
31. Urowitz MB, Bookman AA, Koehler BE, et al. The bimodal mortality pattern of systemic lupus erythematosus. Am J Med 1976; 60: 221-5
32. Frostegard J. Atherosclerosis in patients with autoimmune disorders. Arterioscler Thromb Vasc Biol 2005; 25: 1776-85
33. Manzi S, Meilahn EN, Rairie JE, et al. Age-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus: comparison with the Framingham Study. Am J Epidemiol 1997; 145: 408-15
34. Svenungsson E, Jensen-Urstad K, Heimburger M, et al. Risk factors for cardiovascular disease in systemic lupus erythematosus. Circulation 2001; 104: 1887-93
35. Frostegard J, Wu R, Gillis-Haegerstrand C, et al. Antibodies to endothelial cells in borderline hypertension. Circulation 1998; 98: 1092-8
36. Shoenfeld Y, Gerli R, Doria A, et al. Accelerated atherosclerosis in autoimmune rheumatic diseases. Circulation 2005; 112: 3337-47
37. Su J, Georgiades A, Wu R, et al. Antibodies of IgM subclass to phosphorylcholine and oxidized LDL are protective factors for atherosclerosis in patients with hypertension. Atherosclerosis 2006; 188: 160-6
38. de Faire U, Su J, Hua X, et al. Low levels of IgM antibodies to phosphorylcholine predict cardiovascular disease in 60-year old men: effects on uptake of oxidized LDL in macrophages as a potential mechanism. J Autoimmun 2010; 34: 73-9
39. Frostegard J. Low level natural antibodies against phosphorylcholine: a novel risk marker and potential mechanism in atherosclerosis and cardiovascular disease. Clin Immunol 2010; 134: 47-54
40. Caidahl K, Hartford M, Karlsson T, et al. IgM-phosphorylcholine autoantibodies and outcome in acute coronary syndromes. Int J Cardiol 2013; 167: 464-9
41. Su J, Hua X, Concha H, et al. Natural antibodies against phosphorylcholine as potential protective factors in SLE. Rheumatology (Oxford) 2008; 47: 1144-50
42. Anania C, Gustafsson T, Hua X, et al. Increased prevalence of vulnerable atherosclerotic plaques and low levels of natural IgM antibodies against phosphorylcholine in patients with systemic lupus erythematosus. Arthritis Res Ther 2010; 12: R214
43. Fiskesund R, Su J, Bulatovic I, et al. IgM phosphorylcholine antibodies inhibit cell death and constitute a strong protection marker for atherosclerosis development, particularly in combination with other auto-Antibodies against modified LDL. Results Immunol 2012; 2: 13-18
44. Fiskesund R, Steen J, Amara K, et al. Naturally occurring human phosphorylcholine antibodies are predominantly products of affinity-matured B cells in the adult. J Immunol 2014; 192: 4551-9
45. Roman MJ, Shanker BA, Davis A, et al. Prevalence and correlates of accelerated atherosclerosis in systemic lupus erythematosus. N Engl J Med 2003; 349: 2399-406
46. Doria A, Shoenfeld Y, Wu R, et al. Risk factors for subclinical atherosclerosis in a prospective cohort of patients with systemic lupus erythematosus. Ann Rheum Dis 2003; 62: 1071-7
47. 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
48. Leonard D, Svenungsson E, Sandling JK, et al. Coronary heart disease in systemic lupus erythematosus is associated with interferon regulatory factor-8 gene variants. Circ Cardiovasc Genet 2013; 6: 255-63
49. Iaccarino L, Bettio S, Zen M, et al. Premature coronary heart disease in SLE: can we prevent progression? Lupus 2013; 22: 1232-42
50. Kwee RM, van Oostenbrugge RJ, Hofstra L, et al. Identifying vulnerable carotid plaques by noninvasive imaging. Neurology 2008; 70: 2401-9
51. Mathiesen EB, Bonaa KH, Joakimsen O. Echolucent plaques are associated with high risk of ischemic cerebrovascular events in carotid stenosis: the tromso study. Circulation 2001; 103: 2171-5
52. Tousoulis D, Psarros C, Demosthenous M, et al. Innate and adaptive inflammation as a therapeutic target in vascular disease: the emerging role of statins. J Am Coll Cardiol 2014; 63: 2491-502
53. Tahara N, Kai H, Ishibashi M, et al. Simvastatin attenuates plaque inflammation: evaluation by fluorodeoxyglucose positron emission tomography. J Am Coll Cardiol 2006; 48: 1825-31
54. Tawakol A, Fayad ZA, Mogg R, et al. Intensification of statin therapy results in a rapid reduction in atherosclerotic inflammation: results of a multicenter fluorodeoxyglucose-positron emission tomography/computed tomography feasibility study. J Am Coll Cardiol 2013; 62: 909-17
55. Khan MA, Gallo RM, Renukaradhya GJ, et al. Statins impair CD1d-mediated antigen presentation through the inhibition of prenylation. J Immunol 2009; 182: 4744-50
56. Ghittoni R, Napolitani G, Benati D, et al. Simvastatin inhibits the MHC class II pathway of antigen presentation by impairing Ras superfamily GTPases. Eur J Immunol 2006; 36: 2885-93
57. Ridker PM. Moving Beyond JUPITER. Will Inhibiting Inflammation Reduce Vascular Event Rates? Curr Atheroscler Rep 2013; 15: 295
58. Shepherd J, Cobbe SM, Ford I, et al. Prevention of coronary heart disease with pravastatin in men with hypercholesterolemia. West of Scotland Coronary Prevention Study Group. N Engl J Med 1995; 333: 1301-7
59. Downs JR, Clearfield M, Weis S, et al. Primary prevention of acute coronary events with lovastatin in men and women with average cholesterol levels: results of AFCAPS/TexCAPS. Air Force/Texas Coronary Atherosclerosis Prevention Study. JAMA 1998; 279: 1615-22
60. Kang S, Wu Y, Li X. Effects of statin therapy on the progression of carotid atherosclerosis: a systematic review and meta-Analysis. Atherosclerosis 2004; 177: 433-42
61. Borba EF, Bonfa E. Dyslipoproteinemias in systemic lupus erythematosus: influence of disease, activity, and anticardiolipin antibodies. Lupus 1997; 6: 533-9
62. Willis R, Seif AM, McGwin G Jr, et al. Effects of statins on proinflammatory/prothrombotic biomarkers and on disease activity scores in SLE patients: data from LUMINA (LXXVI), a multi-ethnic US cohort. Clin Exp Rheumatol 2014; 32: 162-7
63. Plazak W, Gryga K, Dziedzic H, et al. Influence of atorvastatin on coronary calcifications and myocardial perfusion defects in systemic lupus erythematosus patients: a prospective, randomized, double-masked, placebo-controlled study. Arthritis Res Ther 2011; 13: R117
64. Ferreira GA, Navarro TP, Telles RW, et al. Atorvastatin therapy improves endothelial-dependent vasodilation in patients with systemic lupus erythematosus: an 8 weeks controlled trial. Rheumatology (Oxford) 2007; 46: 1560-5
65. Ardoin SP, Schanberg LE, Sandborg CI, et al. Secondary analysis of APPLE study suggests atorvastatin may reduce atherosclerosis progression in pubertal lupus patients with higher C reactive protein. Ann Rheum Dis 2014; 73: 557-66
66. Petri MA, Kiani AN, Post W, et al. Lupus Atherosclerosis Prevention Study (LAPS). Ann Rheum Dis 2011; 70: 760-5
67. 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: 322-9
68. Nikpour M, Gladman DD, Urowitz MB. Premature coronary heart disease in systemic lupus erythematosus: what risk factors do we understand? Lupus 2013; 22: 1243-50
69. Steiman AJ, Gladman DD, Ibanez D, Urowitz MB. Prolonged serologically active clinically quiescent systemic lupus erythematosus: frequency and outcome. J Rheumatol 2010; 37: 1822-7
70. Rahman P, Gladman DD, Urowitz MB, et al. The cholesterol lowering effect of antimalarial drugs is enhanced in patients with lupus taking corticosteroid drugs. J Rheumatol 1999; 26: 325-30
71. Penn SK, Kao AH, Schott LL, et al. Hydroxychloroquine and glycemia in women with rheumatoid arthritis and systemic lupus erythematosus. J Rheumatol 2010; 37: 1136-42
72. Landewe RB, van den Borne BE, Breedveld FC, Dijkmans BA. Methotrexate effects in patients with rheumatoid arthritis with cardiovascular comorbidity. Lancet 2000; 355: 1616-17
73. Prodanovich S, Ma F, Taylor JR, et al. Methotrexate reduces incidence of vascular diseases in veterans with psoriasis or rheumatoid arthritis. J Am Acad Dermatol 2005; 52: 262-7
74. Micha R, Imamura F, Wyler von Ballmoos M, et al. Systematic review and meta-Analysis of methotrexate use and risk of cardiovascular disease. Am J Cardiol 2011; 108: 1362-70
75. Bulgarelli A, Martins Dias AA, Caramelli B, et al. Treatment with methotrexate inhibits atherogenesis in cholesterol-fed rabbits. J Cardiovasc Pharmacol 2012; 59: 308-14
76. Hafstrom I, Rohani M, Deneberg S, et al. Effects of low-dose prednisolone on endothelial function, atherosclerosis, and traditional risk factors for atherosclerosis in patients with rheumatoid arthritis-A randomized study. J Rheumatol 2007; 34: 1810-16