Circulation. 2001;104:1887-1893
doi: 10.1161/hc4101.097518
doi: 10.1161/hc4101.097518
(Circulation. 2001;104:1887.)
© 2001 American Heart Association, Inc.
Clinical Investigation and Reports |
Risk Factors for Cardiovascular Disease in Systemic Lupus Erythematosus
From the Department of Rheumatology and Centre for Molecular Medicine (E.S., J.F.), Department of Clinical Physiology (K.J.-U.), Department of Cardiology and King Gustaf V Research Institute 
.S., A.H.), Karolinska Hospital, Stockholm, Sweden; Department of Rheumatology (M.H.), Huddinge University Hospital Huddinge, Sweden; Division of Cardiovascular Epidemiology (U.d.F.), Institute of Environmental Medicine and Cardiovascular Laboratory, Department of Medicine, Karolinska Hospital, Karolinska Institute, Stockholm, Sweden; and Department of Medicine (J.L.W.), University of California, San Diego.
Correspondence to Dr Elisabet Svenungsson, Department of Rheumatology, Karolinska Hospital, 17176 Stockholm, Sweden. E-mail Elisabet.Svenungsson{at}medks.ki.se
Background— Cardiovascular disease (CVD) is overrepresented in patients with systemic lupus erythematosus (SLE). We determined the prevalence of traditional and nontraditional risk factors for CVD in SLE patients with and without CVD compared with controls.
Methods and Results— Twenty-six women (aged 52±8.2 years) with SLE and a history of CVD (SLE cases) were compared with 26 age-matched women with SLE but without manifest CVD (SLE controls) and 26 age-matched population-based control women (population controls). Common carotid intima-media thickness (IMT) was measured by B-mode ultrasound as a surrogate measure of atherosclerosis. SLE cases had increased IMT compared with SLE controls (P=0.03) and population controls (P=0.001), whereas IMT of SLE controls did not differ from population controls. SLE cases had raised plasma concentrations of circulating oxidized LDL (OxLDL; P=0.03), as measured by the monoclonal antibody EO6, and autoantibodies to epitopes of OxLDL (P<0.001); dyslipidemia with raised triglycerides (P<0.001) and lipoprotein(a) (P=0.002) and decreased HDL-cholesterol concentrations (P=0.03); raised -1-antitrypsin (P=0.002), lupus anticoagulant (P=0.007), and homocysteine levels (P=0.03); more frequent osteoporosis (P=0.03); and a higher cumulative prednisolone dose (P=0.05) compared with SLE controls. Disease duration, smoking, blood pressure, body mass index, and diabetes mellitus did not differ significantly between the groups.
Conclusions— set of distinct CVD risk factors separate SLE cases from SLE controls and population controls. If confirmed in a prospective study, they could be used to identify SLE patients at high risk for CVD in order to optimize treatment.
Key Words: cardiovascular diseases • risk factors • therosclerosis • ultrasonics
This article has been cited by other articles:
 |
|
 |
|
  P. Ebner, F. Picard, J. Richter, E. Darrelmann, M. Schneider, B.-E. Strauer, and M. Brehm Accumulation of VEGFR-2+/CD133+ cells and decreased number and impaired functionality of CD34+/VEGFR-2+ cells in patients with SLE Rheumatology, January 1, 2010; 49(1): 63 - 72. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Pertovaara, M. Kahonen, M. Juonala, T. Laitinen, L. Taittonen, T. Lehtimaki, J. S. A. Viikari, O. T. Raitakari, and M. Hurme Autoimmunity and atherosclerosis: the presence of antinuclear antibodies is associated with decreased carotid elasticity in young women. The Cardiovascular Risk in Young Finns Study Rheumatology, December 1, 2009; 48(12): 1553 - 1556. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. J. GOLDBERG, M. B. UROWITZ, D. IBANEZ, M. NIKPOUR, and D. D. GLADMAN Risk Factors for Development of Coronary Artery Disease in Women with Systemic Lupus Erythematosus J Rheumatol, November 1, 2009; 36(11): 2454 - 2461. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 V Bellomio, A Spindler, E Lucero, A Berman, R Sueldo, H Berman, M Santana, M. Molina, V Gongora, G Cassano, et al. Metabolic syndrome in Argentinean patients with systemic lupus erythematosus Lupus, October 1, 2009; 18(11): 1019 - 1025. [Abstract] [PDF]
|
|
|
|
 |
|
 A. Recio-Mayoral, J. C. Mason, J. C. Kaski, M. B. Rubens, O. A. Harari, and P. G. Camici Chronic inflammation and coronary microvascular dysfunction in patients without risk factors for coronary artery disease Eur. Heart J., August 1, 2009; 30(15): 1837 - 1843. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Salvarani, C. D. Bella, L. Cimino, P. Macchioni, D. Formisano, G. Bajocchi, N. Pipitone, M. G. Catanoso, G. Restuccia, A. Ghinoi, et al. Risk factors for severe cranial ischaemic events in an Italian population-based cohort of patients with giant cell arteritis Rheumatology, March 1, 2009; 48(3): 250 - 253. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. R. Batuca, P. R. J. Ames, M. Amaral, C. Favas, D. A. Isenberg, and J. Delgado Alves Anti-atherogenic and anti-inflammatory properties of high-density lipoprotein are affected by specific antibodies in systemic lupus erythematosus Rheumatology, January 1, 2009; 48(1): 26 - 31. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Braun, N. Wade, E. Wakeland, and A. Major Accelerated atherosclerosis is independent of feeding high fat diet in systemic lupus erythematosus-susceptible LDLr-/- mice Lupus, December 1, 2008; 17(12): 1070 - 1078. [Abstract] [PDF]
|
|
|
|
|
|
K de Leeuw, J Blaauw, A. Smit, C. Kallenberg, and M Bijl Vascular responsiveness in the microcirculation of patients with systemic lupus erythematosus is not impaired Lupus, November 1, 2008; 17(11): 1010 - 1017. [Abstract] [PDF]
|
|
|
|
|
|
J. Su, X. Hua, H. Concha, E. Svenungsson, A. Cederholm, and J. Frostegard Natural antibodies against phosphorylcholine as potential protective factors in SLE Rheumatology, August 1, 2008; 47(8): 1144 - 1150. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J Frostegard Systemic lupus erythematosus and cardiovascular disease Lupus, May 1, 2008; 17(5): 364 - 367. [Abstract] [PDF]
|
|
|
|
|
|
R. Telles, C. Lanna, G. Ferreira, A. Souza, T. Navarro, and A. Ribeiro Carotid atherosclerotic alterations in systemic lupus erythematosus patients treated at a Brazilian university setting Lupus, February 1, 2008; 17(2): 105 - 113. [Abstract] [PDF]
|
|
|
|
|
|
S-S. Lee, S. Singh, L. Magder, and M. Petri Predictors of high sensitivity C-reactive protein levels in patients with systemic lupus erythematosus Lupus, February 1, 2008; 17(2): 114 - 123. [Abstract] [PDF]
|
|
|
|
 |
|
 M. J. Roman and J. E. Salmon Cardiovascular Manifestations of Rheumatologic Diseases Circulation, November 13, 2007; 116(20): 2346 - 2355. [Full Text] [PDF]
|
|
|
|
|
|
P.E. Lazzerini, P.L. Capecchi, E. Selvi, S. Lorenzini, S. Bisogno, M. Galeazzi, and F. Laghi Pasini Hyperhomocysteinemia: a cardiovascular risk factor in autoimmune diseases? Lupus, November 1, 2007; 16(11): 852 - 862. [Abstract] [PDF]
|
|
|
|
|
|
A.W.S. de Souza, N.P. Silva, J.F. de Carvalho, V. D'Almeida, M.A.E. Noguti, and E.I. Sato Impact of hypertension and hyperhomocysteinemia on arterial thrombosis in primary antiphospholipid syndrome Lupus, October 1, 2007; 16(10): 782 - 787. [Abstract] [PDF]
|
|
|
|
|
|
K. de Leeuw, R. Graaff, R. de Vries, R. P. Dullaart, A. J. Smit, C. G. Kallenberg, and M. Bijl Accumulation of advanced glycation endproducts in patients with systemic lupus erythematosus Rheumatology, October 1, 2007; 46(10): 1551 - 1556. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Bhatt, R. Handa, G. Gulati, S. Sharma, R. Pandey, P. Aggarwal, L. Ramakrishnan, and S. Shankar Peripheral vascular disease in systemic lupus erythematosus Lupus, September 1, 2007; 16(9): 720 - 723. [Abstract] [PDF]
|
|
|
|
|
|
Y. Ahmad, J. Shelmerdine, H. Bodill, M. Lunt, M. G. Pattrick, L. S. Teh, R. M. Bernstein, M. G. Walker, and I. N. Bruce Subclinical atherosclerosis in systemic lupus erythematosus (SLE): the relative contribution of classic risk factors and the lupus phenotype Rheumatology, June 1, 2007; 46(6): 983 - 988. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J.C. Sachet, E.F. Borba, E. Bonfa, C.G.C. Vinagre, V.M. Silva, and R.C. Maranhao Chloroquine increases low-density lipoprotein removal from plasma in systemic lupus patients Lupus, April 1, 2007; 16(4): 273 - 278. [Abstract] [PDF]
|
|
|
|
|
|
M. Garcia-Carrasco, R.O. Escarcega, J. Perez-Terron, A. Ramirez, M. Munoz-Guarneros, A. Beltran, B. Perez-Cuevas, A. Lopez-Colombo, and R. Cervera Lack of subclinical myocardial ischaemia in Mexican patients with systemic lupus erythematosus without traditional risk factors for coronary artery disease Lupus, April 1, 2007; 16(4): 298 - 301. [Abstract] [PDF]
|
|
|
|
 |
|
 X. Feng, H. Li, A. A. Rumbin, X. Wang, A. La Cava, K. Brechtelsbauer, L. W. Castellani, J. L. Witztum, A. J. Lusis, and B. P. Tsao ApoE-/-Fas-/- C57BL/6 mice: a novel murine model simultaneously exhibits lupus nephritis, atherosclerosis, and osteopenia J. Lipid Res., April 1, 2007; 48(4): 794 - 805. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Torzewski, V. Ochsenhirt, A. L. Kleschyov, M. Oelze, A. Daiber, H. Li, H. Rossmann, S. Tsimikas, K. Reifenberg, F. Cheng, et al. Deficiency of Glutathione Peroxidase-1 Accelerates the Progression of Atherosclerosis in Apolipoprotein E-Deficient Mice Arterioscler Thromb Vasc Biol, April 1, 2007; 27(4): 850 - 857. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M Haubitz Exploring new territory: the move towards individualised treatment Lupus, March 1, 2007; 16(3): 227 - 231. [Abstract] [PDF]
|
|
|
|
|
|
R.-E. W. Kavey, V. Allada, S. R. Daniels, L. L. Hayman, B. W. McCrindle, J. W. Newburger, R. S. Parekh, and J. Steinberger Cardiovascular Risk Reduction in High-Risk Pediatric Patients: A Scientific Statement From the American Heart Association Expert Panel on Population and Prevention Science; the Councils on Cardiovascular Disease in the Young, Epidemiology and Prevention, Nutrition, Physical Activity and Metabolism, High Blood Pressure Research, Cardiovascular Nursing, and the Kidney in Heart Disease; and the Interdisciplinary Working Group on Quality of Care and Outcomes Research: Endorsed by the American Academy of Pediatrics Circulation, December 12, 2006; 114(24): 2710 - 2738. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Z Szekanecz and Y Shoenfeld Lupus and cardiovascular disease: the facts Lupus, November 1, 2006; 15(11_suppl): 3 - 10. [Abstract] [PDF]
|
|
|
|
|
|
M McMahon, J Grossman, W Chen, and B H Hahn Inflammation and the pathogenesis of atherosclerosis in systemic lupus erythematosus Lupus, November 1, 2006; 15(11_suppl): 59 - 69. [Abstract] [PDF]
|
|
|
|
|
|
K De Leeuw, B Freire, A J Smit, H Bootsma, C G Kallenberg, and M Bijl Traditional and non-traditional risk factors contribute to the development of accelerated atherosclerosis in patients with systemic lupus erythematosus Lupus, October 1, 2006; 15(10): 675 - 682. [Abstract] [PDF]
|
|
|
|
|
|
T. K. Tso, W.-N. Huang, H.-Y. Huang, and C.-K. Chang Relationship of plasma interleukin-18 concentrations to traditional and non-traditional cardiovascular risk factors in patients with systemic lupus erythematosus Rheumatology, September 1, 2006; 45(9): 1148 - 1153. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Akagawa, S. Ito, K. Toyoda, Y. Ishii, E. Tatsuda, T. Shibata, S. Yamaguchi, Y. Kawai, K. Ishino, Y. Kishi, et al. Bispecific Abs against modified protein and DNA with oxidized lipids PNAS, April 18, 2006; 103(16): 6160 - 6165. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. C. Hall and N. Dalbeth Disease modification and cardiovascular risk reduction: two sides of the same coin? Rheumatology, December 1, 2005; 44(12): 1473 - 1482. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. N. Bruce 'Not only...but also': factors that contribute to accelerated atherosclerosis and premature coronary heart disease in systemic lupus erythematosus Rheumatology, December 1, 2005; 44(12): 1492 - 1502. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Shoenfeld, R. Gerli, A. Doria, E. Matsuura, M. M. Cerinic, N. Ronda, L. J. Jara, M. Abu-Shakra, P. L. Meroni, and Y. Sherer Accelerated Atherosclerosis in Autoimmune Rheumatic Diseases Circulation, November 22, 2005; 112(21): 3337 - 3347. [Full Text] [PDF]
|
|
|
|
|
|
C R. Cardoso, M A. Sales, J A. Papi, and G F Salles QT-interval parameters are increased in systemic lupus erythematosus patients Lupus, October 1, 2005; 14(10): 846 - 852. [Abstract] [PDF]
|
|
|
|
|
|
K. T. Ho, C. W. Ahn, G. S. Alarcon, B. A. Baethge, F. K. Tan, J. Roseman, H. M. Bastian, B. J. Fessler, G. McGwin Jr, L. M. Vila, et al. Systemic lupus erythematosus in a multiethnic cohort (LUMINA): XXVIII. Factors predictive of thrombotic events Rheumatology, October 1, 2005; 44(10): 1303 - 1307. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I N Bruce Atherogenesis and autoimmune disease: the model of lupus Lupus, September 1, 2005; 14(9): 687 - 690. [Abstract] [PDF]
|
|
|
|
|
|
J. Frostegard Atherosclerosis in Patients With Autoimmune Disorders Arterioscler Thromb Vasc Biol, September 1, 2005; 25(9): 1776 - 1785. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 I E M Bultink, T Teerlink, J A Heijst, B A C Dijkmans, and A E Voskuyl Raised plasma levels of asymmetric dimethylarginine are associated with cardiovascular events, disease activity, and organ damage in patients with systemic lupus erythematosus Ann Rheum Dis, September 1, 2005; 64(9): 1362 - 1365. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Jimenez, M. A. Garcia-Criado, D. Tassies, J. C. Reverter, R. Cervera, M. R. Gilabert, D. Zambon, E. Ros, C. Bru, and J. Font Preclinical vascular disease in systemic lupus erythematosus and primary antiphospholipid syndrome Rheumatology, June 1, 2005; 44(6): 756 - 761. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Schneider, J. L. Witztum, S. G. Young, E. H. Ludwig, E. R. Miller, S. Tsimikas, L. K. Curtiss, S. M. Marcovina, J. M. Taylor, R. M. Lawn, et al. High-level lipoprotein [a] expression in transgenic mice: evidence for oxidized phospholipids in lipoprotein [a] but not in low density lipoproteins J. Lipid Res., April 1, 2005; 46(4): 769 - 778. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P R J Ames, A Margarita, K B Sokoll, M Weston, and V Brancaccio Premature atherosclerosis in primary antiphospholipid syndrome: preliminary data Ann Rheum Dis, February 1, 2005; 64(2): 315 - 317. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Cederholm, E. Svenungsson, K. Jensen-Urstad, C. Trollmo, A.-K. Ulfgren, J. Swedenborg, G.-Z. Fei, and J. Frostegard Decreased Binding of Annexin V to Endothelial Cells: A Potential Mechanism in Atherothrombosis of Patients With Systemic Lupus Erythematosus Arterioscler Thromb Vasc Biol, January 1, 2005; 25(1): 198 - 203. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M.-K. Chang, C. J. Binder, Y. I. Miller, G. Subbanagounder, G. J. Silverman, J. A. Berliner, and J. L. Witztum Apoptotic Cells with Oxidation-specific Epitopes Are Immunogenic and Proinflammatory J. Exp. Med., December 6, 2004; 200(11): 1359 - 1370. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B Siripaitoon, M Osiri, V Vongthavaravat, S Akkasilpa, and U Deesomchok The prevalence of dyslipoproteinemia in Thai patients with systemic lupus erythematosus Lupus, December 1, 2004; 13(12): 961 - 968. [Abstract] [PDF]
|
|
|
|
|
|
Y. Shoenfeld, R. Wu, L. D. Dearing, and E. Matsuura Are Anti-Oxidized Low-Density Lipoprotein Antibodies Pathogenic or Protective? Circulation, October 26, 2004; 110(17): 2552 - 2558. [Full Text] [PDF]
|
|
|
|
|
|
M.-L. Liu, K. Ylitalo, R. Salonen, J. T. Salonen, and M.-R. Taskinen Circulating Oxidized Low-Density Lipoprotein and Its Association With Carotid Intima-Media Thickness in Asymptomatic Members of Familial Combined Hyperlipidemia Families Arterioscler Thromb Vasc Biol, August 1, 2004; 24(8): 1492 - 1497. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Pullmann Jr, M. Skerenova, J. Lukac, J. Hybenova, V. Melus, P. Kubisz, J. Rovensky, and R. Pullmann Factor V Leiden and Prothrombin G20210A Mutations and the Risk of Atherothrombotic Events in Systemic Lupus Erythematosus Clinical and Applied Thrombosis/Hemostasis, July 1, 2004; 10(3): 233 - 238. [Abstract] [PDF]
|
|
|
|
|
|
R. Bessant, A. Hingorani, L. Patel, A. MacGregor, D. A. Isenberg, and A. Rahman Risk of coronary heart disease and stroke in a large British cohort of patients with systemic lupus erythematosus Rheumatology, July 1, 2004; 43(7): 924 - 929. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. J. Roman, B.-A. Shanker, A. Davis, M. D. Lockshin, L. Sammaritano, R. Simantov, M. K. Crow, J. E. Schwartz, S. A. Paget, R. B. Devereux, et al. Prevalence and Correlates of Accelerated Atherosclerosis in Systemic Lupus Erythematosus N. Engl. J. Med., December 18, 2003; 349(25): 2399 - 2406. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Asanuma, A. Oeser, A. K. Shintani, E. Turner, N. Olsen, S. Fazio, M. F. Linton, P. Raggi, and C. M. Stein Premature Coronary-Artery Atherosclerosis in Systemic Lupus Erythematosus N. Engl. J. Med., December 18, 2003; 349(25): 2407 - 2415. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A Doria, Y Shoenfeld, R Wu, P F Gambari, M Puato, A Ghirardello, B Gilburd, S Corbanese, M Patnaik, S Zampieri, et al. Risk factors for subclinical atherosclerosis in a prospective cohort of patients with systemic lupus erythematosus Ann Rheum Dis, November 1, 2003; 62(11): 1071 - 1077. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K Manger, M Kusus, C Forster, D Ropers, W G Daniel, J R Kalden, S Achenbach, and B Manger Factors associated with coronary artery calcification in young female patients with SLE Ann Rheum Dis, September 1, 2003; 62(9): 846 - 850. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Schattner and M. H. Liang The Cardiovascular Burden of Lupus: A Complex Challenge Arch Intern Med, July 14, 2003; 163(13): 1507 - 1510. [Full Text] [PDF]
|
|
|
|
|
|
E Svenungsson, G-Z Fei, K Jensen-Urstad, U de Faire, A Hamsten, and J Frostegard TNF-{alpha}: a link between hypertriglyceridaemia and inflammation in SLE patients with cardiovascular disease Lupus, June 1, 2003; 12(6): 454 - 461. [Abstract] [PDF]
|
|
|
|
|
|
S. L. Nuttall, S. Heaton, M. K. Piper, U. Martin, and C. Gordon Cardiovascular risk in systemic lupus erythematosus--evidence of increased oxidative stress and dyslipidaemia Rheumatology, June 1, 2003; 42(6): 758 - 762. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K Jensen-Urstad, E Svenungsson, U de Faire, A Silveira, J L Witztum, A Hamsten, and J Frostegard Cardiac valvular abnormalities are frequent in systemic lupus erythematosus patients with manifest arterial disease Lupus, November 1, 2002; 11(11): 744 - 752. [Abstract] [PDF]
|
|
|
|
 |
|
 S. Bulusu, P. H Dessein, A. E Stanwix, and L. A Malcolm Rational, cost effective use of investigations BMJ, July 27, 2002; 325(7357): 222 - 222. [Full Text]
|
|
|
|
|
|
P. Thiagarajan Atherosclerosis, Autoimmunity, and Systemic Lupus Erythematosus Circulation, October 16, 2001; 104(16): 1876 - 1877. [Full Text] [PDF]
|
|