J Korean Med Sci.  2020 Jun;35(21):e139. 10.3346/jkms.2020.35.e139.

Anti-Sm Antibody, Damage Index, and Corticosteroid Use Are Associated with Cardiac Involvement in Systemic Lupus Erythematosus: Data from a Prospective Registry Study

• Choe JY
• Lee SS
• Kwak SG
• Kim SK

• KMID: 2502240
• DOI: http://doi.org/10.3346/jkms.2020.35.e139

Abstract

Background
Disease-specific factors that predispose patients to diverse cardiac diseases in systemic lupus erythematosus (SLE) have been established. The aim of this study was to identify risk factors for cardiac involvement in patients with SLE drawn from the Korean Lupus Network (KORNET) registry.
Methods
A total of 437 patients with SLE recruited from the KORNET registry were included in the analysis. The Cox proportional hazard model was used to identify risk factors for the development of cardiac involvement during the follow-up period. The hazard ratios for risk factors of cardiac involvement were assessed using Kaplan-Meier curves and log-rank test.
Results
Of 437 patients with SLE, 12 patients (2.7%) developed new cardiac involvement during a median follow-up period of 47.6 months. Frequencies in men and in patients with anti-Sm antibody, anti-Ro antibody, and at least one Systemic Lupus International Collaborating Clinics/American College of Rheumatology damage index (SDI) score in patients with cardiac involvement were higher, compared to those without cardiac involvement (P < 0.001, P = 0.026, P = 0.015, and P < 0.001, respectively). Men gender, older age, anti-Sm antibody, SDI, and corticosteroid dosage were potent predictors for cardiac involvement in patients with SLE in the determination of risk factors for cardiac involvement. Men, anti-Sm antibody positivity, and SDI ≥ 1 increased incidence rates of cardiac involvement for (P < 0.001, P = 0.036, and P < 0.001, respectively).
Conclusion
The results of this study reveal that SLE-related factors such as anti-Sm antibody, SDI, and corticosteroid dosage at baseline are risk factors for cardiac involvement in SLE.

Keyword

Systemic Lupus Erythematous; Cardiovascular Disease; Autoimmunity; Steroid

Figure

• 

  Fig. 1 Kaplan-Meier curves for cardiovascular diseases according to variables at baseline over time.SDI = Systemic Lupus International Collaborating Clinics/American College of Rheumatology damage index.

Reference

1. Lisnevskaia L, Murphy G, Isenberg D. Systemic lupus erythematosus. Lancet. 2014; 384(9957):1878–1888. PMID: 24881804.

2. Tsokos GC. Systemic lupus erythematosus. N Engl J Med. 2011; 365(22):2110–2121. PMID: 22129255.

3. Borchers AT, Keen CL, Shoenfeld Y, Gershwin ME. Surviving the butterfly and the wolf: mortality trends in systemic lupus erythematosus. Autoimmun Rev. 2004; 3(6):423–453. PMID: 15351310.

4. Aviña-Zubieta JA, To F, Vostretsova K, De Vera M, Sayre EC, Esdaile JM. Risk of myocardial infarction and stroke in newly diagnosed systemic lupus erythematosus: a general population-based study. Arthritis Care Res (Hoboken). 2017; 69(6):849–856. PMID: 28129475.

5. Tselios K, Gladman DD, Su J, Ace O, Urowitz MB. Evolution of risk factors for atherosclerotic cardiovascular events in systemic lupus erythematosus: a longterm prospective study. J Rheumatol. 2017; 44(12):1841–1849. PMID: 29093154.

6. Kim SK, Choe JY, Lee SS. Self-reported physical activity is associated with lupus nephritis in systemic lupus erythematosus: data from KORean Lupus Network (KORNET) registry. Yonsei Med J. 2018; 59(7):857–864. PMID: 30091319.

7. Koh JH, Park EK, Lee HN, Kim Y, Kim GT, Suh YS, et al. Clinical characteristics and survival of 413 patients with systemic lupus erythematosus in southeastern areas of South Korea: a multicenter retrospective cohort study. Int J Rheum Dis. 2020; 23(1):92–100. PMID: 31802639.

8. Petri M, Perez-Gutthann S, Spence D, Hochberg MC. Risk factors for coronary artery disease in patients with systemic lupus erythematosus. Am J Med. 1992; 93(5):513–519. PMID: 1442853.

9. Urowitz MB, Ibañez D, Gladman DD. Atherosclerotic vascular events in a single large lupus cohort: prevalence and risk factors. J Rheumatol. 2007; 34(1):70–75. PMID: 17117488.

10. Sinicato NA, da Silva Cardoso PA, Appenzeller S. Risk factors in cardiovascular disease in systemic lupus erythematosus. Curr Cardiol Rev. 2013; 9(1):15–19. PMID: 23463953.

11. Manzi S, Meilahn EN, Rairie JE, Conte CG, Medsger TA Jr, Jansen-McWilliams L, 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(5):408–415. PMID: 9048514.

12. Teixeira V, Tam LS. Novel insights in systemic lupus erythematosus and atherosclerosis. Front Med (Lausanne). 2018; 4:262. PMID: 29435447.

13. Lim SY, Bae EH, Han KD, Jung JH, Choi HS, Kim HY, et al. Systemic lupus erythematosus is a risk factor for cardiovascular disease: a nationwide, population-based study in Korea. Lupus. 2018; 27(13):2050–2056. PMID: 30282562.

14. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1982; 25(11):1271–1277. PMID: 7138600.

15. Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1997; 40(9):1725.

16. Steering Committee. The Asia-Pacific perspective: Redefining Obesity and Its Treatment. Melbourne: International Diabetes Institute;2000.

17. Rees F, Doherty M, Grainge MJ, Lanyon P, Davenport G, Zhang W. Mortality in systemic lupus erythematosus in the United Kingdom 1999–2012. Rheumatology (Oxford). 2016; 55(5):854–860. PMID: 26748350.

18. Yee CS, Su L, Toescu V, Hickman R, Situnayake D, Bowman S, et al. Birmingham SLE cohort: outcomes of a large inception cohort followed for up to 21 years. Rheumatology (Oxford). 2015; 54(5):836–843. PMID: 25323056.

19. Kiani AN, Vogel-Claussen J, Arbab-Zadeh A, Magder LS, Lima J, Petri M. Semiquantified noncalcified coronary plaque in systemic lupus erythematosus. J Rheumatol. 2012; 39(12):2286–2293. PMID: 23027889.

20. Toloza SM, Uribe AG, McGwin G Jr, Alarcón GS, Fessler BJ, Bastian HM, et al. Systemic lupus erythematosus in a multiethnic US cohort (LUMINA). XXIII. Baseline predictors of vascular events. Arthritis Rheum. 2004; 50(12):3947–3957. PMID: 15593203.

21. Gustafsson J, Gunnarsson I, Börjesson O, Pettersson S, Möller S, Fei GZ, et al. Predictors of the first cardiovascular event in patients with systemic lupus erythematosus - a prospective cohort study. Arthritis Res Ther. 2009; 11(6):R186. PMID: 20003285.

22. Lockshin M, Tenedios F, Petri M, McCarty G, Forastiero R, Krilis S, et al. Cardiac disease in the antiphospholipid syndrome: recommendations for treatment. Committee consensus report. Lupus. 2003; 12(7):518–523. PMID: 12892391.

23. Haque S, Gordon C, Isenberg D, Rahman A, Lanyon P, Bell A, 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(2):322–329. PMID: 19955047.

24. Rahman P, Gladman DD, Urowitz MB, Hallett D, Tam LS. Early damage as measured by the SLICC/ACR damage index is a predictor of mortality in systemic lupus erythematosus. Lupus. 2001; 10(2):93–96. PMID: 11237132.

25. Ho KT, Ahn CW, Alarcón GS, Baethge BA, Tan FK, Roseman J, et al. Systemic lupus erythematosus in a multiethnic cohort (LUMINA): XXVIII. Factors predictive of thrombotic events. Rheumatology (Oxford). 2005; 44(10):1303–1307. PMID: 16030085.

26. Tan TC, Fang H, Magder LS, Petri MA. Differences between male and female systemic lupus erythematosus in a multiethnic population. J Rheumatol. 2012; 39(4):759–769. PMID: 22382348.

27. Stefanidou S, Benos A, Galanopoulou V, Chatziyannis I, Kanakoudi F, Aslanidis S, et al. Clinical expression and morbidity of systemic lupus erythematosus during a post-diagnostic 5-year follow-up: a male:female comparison. Lupus. 2011; 20(10):1090–1094. PMID: 21700658.

28. Garcia MA, Marcos JC, Marcos AI, Pons-Estel BA, Wojdyla D, Arturi A, et al. Male systemic lupus erythematosus in a Latin-American inception cohort of 1214 patients. Lupus. 2005; 14(12):938–946. PMID: 16425573.

29. Boodhoo KD, Liu S, Zuo X. Impact of sex disparities on the clinical manifestations in patients with systemic lupus erythematosus: a systematic review and meta-analysis. Medicine (Baltimore). 2016; 95(29):e4272. PMID: 27442661.

30. Hwang J, Lee J, Ahn JK, Park EJ, Cha HS, Koh EM. Clinical characteristics of male and female Korean patients with systemic lupus erythematosus: a comparative study. Korean J Intern Med. 2015; 30(2):242–249. PMID: 25750567.

31. Penn SK, Kao AH, Schott LL, Elliott JR, Toledo FG, Kuller L, et al. Hydroxychloroquine and glycemia in women with rheumatoid arthritis and systemic lupus erythematosus. J Rheumatol. 2010; 37(6):1136–1142. PMID: 20436082.

32. Singh AG, Crowson CS, Singh S, Denis M, Davis P, Maradit-Kremers H, et al. Risk of cerebrovascular accidents and ischemic heart disease in cutaneous lupus erythematosus: a population-based cohort study. Arthritis Care Res (Hoboken). 2016; 68(11):1664–1670. PMID: 27015109.