Risk factors for cardiovascular mortality in patients with systemic lupus erythematosus, a prospective cohort study

Arthritis Research and Therapy

Volumn 14, Issue 2, 2012, Pages

  Gustafsson, Johanna T ^a   Simard, Julia F ^b   Gunnarsson, Iva ^a   Elvin, Kerstin ^a   Lundberg, Ingrid E ^a   Hansson, Lars Olof ^a   Larsson, Anders ^c   Svenungsson, Elisabet ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UPPSALA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 1 ANTITRYPSIN; BETA2 GLYCOPROTEIN 1 ANTIBODY; BIOLOGICAL MARKER; C REACTIVE PROTEIN; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C4; CYSTATIN C; FIBRINOGEN; INTERLEUKIN 6; PHOSPHOLIPID ANTIBODY; SERUM AMYLOID A; VASCULAR CELL ADHESION MOLECULE 1; VON WILLEBRAND FACTOR; CST3 PROTEIN, HUMAN;

ADULT; AGE; AGED; ARTERY DISEASE; ARTICLE; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CAUSE OF DEATH; COHORT ANALYSIS; DISEASE SEVERITY; FEMALE; FOLLOW UP; HUMAN; INFLAMMATION; MAJOR CLINICAL STUDY; MALE; MORBIDITY; MORTALITY; PROGNOSIS; PROSPECTIVE STUDY; RISK FACTOR; SCORING SYSTEM; SMOKING; STANDARDIZED MORTALITY RATIO; SYSTEMIC CORONARY RISK EVALUATION; SYSTEMIC LUPUS ERYTHEMATOSUS; BLOOD; MIDDLE AGED; REGISTER; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; BIOLOGICAL MARKERS; CARDIOVASCULAR DISEASES; COHORT STUDIES; CYSTATIN C; FEMALE; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MIDDLE AGED; PROSPECTIVE STUDIES; REGISTRIES; RISK FACTORS;

EID: 84857676725     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar3759     Document Type: Article

References (49)

1. Ahmad Y, Shelmerdine J, Bodill H, Lunt M, Pattrick MG, Teh LS, Bernstein RM, Walker MG, Bruce IN. Subclinical atherosclerosis in systemic lupus erythematosus (SLE): the relative contribution of classic risk factors and the lupus phenotype. Rheumatology (Oxford) 2007, 46:983-988.
2. Manzi S, Selzer F, Sutton-Tyrrell K, Fitzgerald SG, Rairie JE, Tracy RP, Kuller LH. Prevalence and risk factors of carotid plaque in women with systemic lupus erythematosus. Arthritis Rheum 1999, 42:51-60. 10.1002/1529-0131(199901)42:1<51::AID-ANR7>3.0.CO;2-D, 9920014.
3. Roman MJ, Shanker BA, Davis A, Lockshin MD, Sammaritano L, Simantov R, Crow MK, Schwartz JE, Paget SA, Devereux RB, Salmon JE. Prevalence and correlates of accelerated atherosclerosis in systemic lupus erythematosus. N Engl J Med 2003, 349:2399-2406. 10.1056/NEJMoa035471, 14681505.
4. de Leeuw K, Freire B, Smit AJ, Bootsma H, Kallenberg CG, Bijl M. Traditional and non-traditional risk factors contribute to the development of accelerated atherosclerosis in patients with systemic lupus erythematosus. Lupus 2006, 15:675-682. 10.1177/0961203306069972, 17120595.
5. Merrell M, Shulman LE. Determination of prognosis in chronic disease, illustrated by systemic lupus erythematosus. J Chronic Dis 1955, 1:12-32. 10.1016/0021-9681(55)90018-7, 13233308.
6. Kasitanon N, Magder LS, Petri M. Predictors of survival in systemic lupus erythematosus. Medicine (Baltimore) 2006, 85:147-156.
7. Funauchi M, Shimadzu H, Tamaki C, Yamagata T, Nozaki Y, Sugiyama M, Ikoma S, Kinoshita K. Survival study by organ disorders in 306 Japanese patients with systemic lupus erythematosus: results from a single center. Rheumatol Int 2007, 27:243-249.
8. Urowitz MB, Gladman DD, Tom BD, Ibanez D, Farewell VT. Changing patterns in mortality and disease outcomes for patients with systemic lupus erythematosus. J Rheumatol 2008, 35:2152-2158. 10.3899/jrheum.080214, 18793004.
9. Mok CC, Kwok CL, Ho LY, Chan PT, Yip SF. Life expectancy, standardized mortality ratios, and causes of death in six rheumatic diseases in Hong Kong, China. Arthritis Rheum 2011, 63:1182-1189. 10.1002/art.30277, 21391198.
10. Jacobsen S, Petersen J, Ullman S, Junker P, Voss A, Rasmussen JM, Tarp U, Poulsen LH, van Overeem Hansen G, Skaarup B, Hansen TM, Podenphant J, Halberg P. A multicentre study of 513 Danish patients with systemic lupus erythematosus. II. Disease mortality and clinical factors of prognostic value. Clin Rheumatol 1998, 17:478-484. 10.1007/BF01451283, 9890675.
11. Chambers SA, Allen E, Rahman A, Isenberg D. Damage and mortality in a group of British patients with systemic lupus erythematosus followed up for over 10 years. Rheumatology (Oxford) 2009, 48:673-675.
12. Rabbani MA, Habib HB, Islam M, Ahmad B, Majid S, Saeed W, Shah SM, Ahmad A. Survival analysis and prognostic indicators of systemic lupus erythematosus in Pakistani patients. Lupus 2009, 18:848-855. 10.1177/0961203309103410, 19578112.
13. Wadee S, Tikly M, Hopley M. Causes and predictors of death in South Africans with systemic lupus erythematosus. Rheumatology (Oxford) 2007, 46:1487-1491.
14. Bjornadal L, Yin L, Granath F, Klareskog L, Ekbom A. Cardiovascular disease a hazard despite improved prognosis in patients with systemic lupus erythematosus: results from a Swedish population based study 1964-95. J Rheumatol 2004, 31:713-719.
15. Bernatsky S, Boivin JF, Joseph L, Manzi S, Ginzler E, Gladman DD, Urowitz M, Fortin PR, Petri M, Barr S, Gordon C, Bae SC, Isenberg D, Zoma A, Aranow C, Dooley MA, Nived O, Sturfelt G, Steinsson K, Alarcon G, Senecal JL, Zummer M, Hanly J, Ensworth S, Pope J, Edworthy S, Rahman A, Sibley J, El-Gabalawy H, McCarthy T, et al. Mortality in systemic lupus erythematosus. Arthritis Rheum 2006, 54:2550-2557. 10.1002/art.21955, 16868977.
16. Moss KE, Ioannou Y, Sultan SM, Haq I, Isenberg DA. Outcome of a cohort of 300 patients with systemic lupus erythematosus attending a dedicated clinic for over two decades. Ann Rheum Dis 2002, 61:409-413. 10.1136/ard.61.5.409, 1754082, 11959764.
17. Stahl-Hallengren C, Jonsen 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, 27:685-691.
18. Reveille JD, Bartolucci A, Alarcon GS. Prognosis in systemic lupus erythematosus. Negative impact of increasing age at onset, black race, and thrombocytopenia, as well as causes of death. Arthritis Rheum 1990, 33:37-48. 10.1002/art.1780330105, 2302266.
19. Abu-Shakra M, Urowitz MB, Gladman DD, Gough J. Mortality studies in systemic lupus erythematosus. Results from a single center. II. Predictor variables for mortality. J Rheumatol 1995, 22:1265-1270.
20. Manger K, Manger B, Repp R, Geisselbrecht M, Geiger A, Pfahlberg A, Harrer T, Kalden JR. Definition of risk factors for death, end stage renal disease, and thromboembolic events in a monocentric cohort of 338 patients with systemic lupus erythematosus. Ann Rheum Dis 2002, 61:1065-1070. 10.1136/ard.61.12.1065, 1753955, 12429536.
21. Doria A, Iaccarino L, Ghirardello A, Zampieri S, Arienti S, Sarzi-Puttini P, Atzeni F, Piccoli A, Todesco S. Long-term prognosis and causes of death in systemic lupus erythematosus. Am J Med 2006, 119:700-706. 10.1016/j.amjmed.2005.11.034, 16887417.
22. Conroy RM, Pyorala K, Fitzgerald AP, Sans S, Menotti A, De Backer G, De Bacquer D, Ducimetiere P, Jousilahti P, Keil U, Njolstad I, Oganov RG, Thomsen T, Tunstall-Pedoe H, Tverval A, Wedel H, Whincup P, Wilhelmsen L, Graham IM. Estimation of ten-year risk of fatal cardiovascular disease in Europe: the SCORE project. Eur Heart J 2003, 24:987-1003. 10.1016/S0195-668X(03)00114-3, 12788299.
23. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, Schaller JG, Talal N, Winchester RJ. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982, 25:1271-1277. 10.1002/art.1780251101, 7138600.
24. Liang MH, Socher SA, Roberts WN, Esdaile JM. Measurement of systemic lupus erythematosus activity in clinical research. Arthritis Rheum 1988, 31:817-825. 10.1002/art.1780310701, 3293570.
25. Gladman D, Ginzler E, Goldsmith C, Fortin P, Liang M, Urowitz M, Bacon P, Bombardieri S, Hanly J, Hay E, Isenberg D, Jones J, Kalunian K, Maddison P, Nived O, Petri M, Richter M, Sanchez-Guerrero J, Snaith M, Sturfelt G, Symmons D, Zoma A. The development and initial validation of the Systemic Lupus International Collaborating Clinics/American College of Rheumatology damage index for systemic lupus erythematosus. Arthritis Rheum 1996, 39:363-369. 10.1002/art.1780390303, 8607884.
26. Gustafsson J, Gunnarsson I, Borjesson O, Pettersson S, Moller S, Fei GZ, Elvin K, Simard JF, Hansson LO, Lundberg IE, Larsson A, Svenungsson E. Predictors of the first cardiovascular event in patients with systemic lupus erythematosus - a prospective cohort study. Arthritis Res Ther 2009, 11:R186. 10.1186/ar2878, 3003532, 20003285.
27. Heartscore. , http://www.heartscore.org
28. Jacobsen S, Petersen J, Ullman S, Junker P, Voss A, Rasmussen JM, Tarp U, Poulsen LH, van Overeem Hansen G, Skaarup B, Hansen TM, Podenphant J, Halberg P. Mortality and causes of death of 513 Danish patients with systemic lupus erythematosus. Scand J Rheumatol 1999, 28:75-80. 10.1080/030097499442522, 10229135.
29. Cervera R, Khamashta MA, Font J, Sebastiani GD, Gil A, Lavilla P, Mejia JC, Aydintug AO, Chwalinska-Sadowska H, de Ramon E, Fernandez-Nebro A, Galeazzi M, Valen M, Mathieu A, Houssiau F, Caro N, Alba P, Ramos-Casals M, Ingelmo M, Hughes GR. Morbidity and mortality in systemic lupus erythematosus during a 10-year period: a comparison of early and late manifestations in a cohort of 1,000 patients. Medicine (Baltimore) 2003, 82:299-308.
30. Nived O, Jonsen A, Bengtsson AA, Bengtsson C, Sturfelt G. High predictive value of the Systemic Lupus International Collaborating Clinics/American College of Rheumatology damage index for survival in systemic lupus erythematosus. J Rheumatol 2002, 29:1398-1400.
31. Shlipak MG, Weekley CC, Li Y, Hansson LO, Larsson A, Whooley M. Comparison of cardiovascular prognosis by 3 serum cystatin C methods in the heart and soul study. Clin Chem 2011, 57:737-745. 10.1373/clinchem.2010.158915, 21310869.
32. Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D. A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. Modification of Diet in Renal Disease Study Group. Ann Intern Med 1999, 130:461-470.
33. Faurschou M, Dreyer L, Kamper AL, Starklint H, Jacobsen S. Long-term mortality and renal outcome in a cohort of 100 patients with lupus nephritis. Arthritis Care Res (Hoboken) 2010, 62:873-880.
34. Pucci L, Triscornia S, Lucchesi D, Fotino C, Pellegrini G, Pardini E, Miccoli R, Del Prato S, Penno G. Cystatin C and estimates of renal function: searching for a better measure of kidney function in diabetic patients. Clin Chem 2007, 53:480-488. 10.1373/clinchem.2006.076042, 17259236.
35. Hsu CY, Chertow GM, Curhan GC. Methodological issues in studying the epidemiology of mild to moderate chronic renal insufficiency. Kidney Int 2002, 61:1567-1576. 10.1046/j.1523-1755.2002.00299.x, 11967006.
36. Risch L, Herklotz R, Blumberg A, Huber AR. Effects of glucocorticoid immunosuppression on serum cystatin C concentrations in renal transplant patients. Clin Chem 2001, 47:2055-2059.
37. Keller CR, Odden MC, Fried LF, Newman AB, Angleman S, Green CA, Cummings SR, Harris TB, Shlipak MG. Kidney function and markers of inflammation in elderly persons without chronic kidney disease: the health, aging, and body composition study. Kidney Int 2007, 71:239-244. 10.1038/sj.ki.5002042, 17183246.
38. Lee M, Saver JL, Huang WH, Chow J, Chang KH, Ovbiagele B. Impact of elevated cystatin C level on cardiovascular disease risk in predominantly high cardiovascular risk populations: a meta-analysis. Circ Cardiovasc Qual Outcomes 2010, 3:675-683. 10.1161/CIRCOUTCOMES.110.957696, 20923994.
39. Wu CK, Lin JW, Caffrey JL, Chang MH, Hwang JJ, Lin YS. Cystatin C and long-term mortality among subjects with normal creatinine-based estimated glomerular filtration rates: NHANES III (Third National Health and Nutrition Examination Survey). J Am Coll Cardiol 2010, 56:1930-1936. 10.1016/j.jacc.2010.04.069, 21109116.
40. Svenungsson E, Cederholm A, Jensen-Urstad K, Fei GZ, de Faire U, Frostegard J. Endothelial function and markers of endothelial activation in relation to cardiovascular disease in systemic lupus erythematosus. Scand J Rheumatol 2008, 37:352-359. 10.1080/03009740802007514, 18666029.
41. Kaptoge S, Di Angelantonio E, Lowe G, Pepys MB, Thompson SG, Collins R, Danesh J. C-reactive protein concentration and risk of coronary heart disease, stroke, and mortality: an individual participant meta-analysis. Lancet 2010, 375:132-140. 3162187, 20031199.
42. Danesh J, Lewington S, Thompson SG, Lowe GD, Collins R, Kostis JB, Wilson AC, Folsom AR, Wu K, Benderly M, Goldbourt U, Willeit J, Kiechl S, Yarnell JW, Sweetnam PM, Elwood PC, Cushman M, Psaty BM, Tracy RP, Tygbjaerg-Hansen A, Haverkate F, de Maat MP, Fowkes FG, Lee AJ, Smith FB, Salomaa V, Harald K, Rasi R, Vahtera E, Jousilahti P, et al. Plasma fibrinogen level and the risk of major cardiovascular diseases and nonvascular mortality: an individual participant meta-analysis. Jama 2005, 294:1799-1809.
43. Kao AH, Wasko MC, Krishnaswami S, Wagner J, Edmundowicz D, Shaw P, Cunningham AL, Danchenko N, Sutton-Tyrrell K, Tracy RP, Kuller LH, Manzi S. C-reactive protein and coronary artery calcium in asymptomatic women with systemic lupus erythematosus or rheumatoid arthritis. Am J Cardiol 2008, 102:755-760. 10.1016/j.amjcard.2008.04.059, 2563802, 18774002.
44. Toloza SM, Uribe AG, McGwin G, Alarcon GS, Fessler BJ, Bastian HM, Vila LM, Wu R, Shoenfeld Y, Roseman JM, Reveille JD. Systemic lupus erythematosus in a multiethnic US cohort (LUMINA). XXIII. Baseline predictors of vascular events. Arthritis Rheum 2004, 50:3947-3957. 10.1002/art.20622, 15593203.
45. Svenungsson E, Jensen-Urstad K, Heimburger M, Silveira A, Hamsten A, de Faire U, Witztum JL, Frostegard J. Risk factors for cardiovascular disease in systemic lupus erythematosus. Circulation 2001, 104:1887-1893. 10.1161/hc4101.097518, 11602489.
46. Miyakis S, Lockshin MD, Atsumi T, Branch DW, Brey RL, Cervera R, Derksen RH, PG DEG, Koike T, Meroni PL, Reber G, Shoenfeld Y, Tincani A, Vlachoyiannopoulos PG, Krilis SA. International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). J Thromb Haemost 2006, 4:295-306. 10.1111/j.1538-7836.2006.01753.x, 16420554.
47. Petri M. Update on anti-phospholipid antibodies in SLE: the Hopkins' Lupus Cohort. Lupus 2010, 19:419-423. 10.1177/0961203309360541, 20353980.
48. Seleznick MJ, Fries JF. Variables associated with decreased survival in systemic lupus erythematosus. Semin Arthritis Rheum 1991, 21:73-80. 10.1016/0049-0172(91)90040-7, 1749941.
49. Kim WU, Min JK, Lee SH, Park SH, Cho CS, Kim HY. Causes of death in Korean patients with systemic lupus erythematosus: a single center retrospective study. Clin Exp Rheumatol 1999, 17:539-545.