Clinical Rheumatology

, Volume 35, Issue 10, pp 2437–2448 | Cite as

Heart involvement in systemic lupus erythematosus: a systemic review and meta-analysis

  • Junzhe Chen
  • Ying Tang
  • Mingsheng Zhu
  • Anping XuEmail author
Original Article


Cardiovascular diseases are one of the most important causes of the disability and mortality in patients with systemic lupus erythematosus (SLE). The present study examined the cardiac abnormalities in patients with SLE by echocardiography. Case-control studies were obtained by searching PubMed MEDLINE, Embase, and MD Consult. Systemic review and meta-analysis were performed to assess the cardiac abnormalities based on the changes in the echocardiography in patients with SLE. Twenty-two studies including 1117 SLE patients and 901 healthy controls were enrolled into this study. We found that patients with SLE developed the pericardial effusion (odds ratio (OR) (95 % confidence interval (CI)) 30.52 (9.70–96.02); p < 0.00001) and the combined valvular alterations (OR (95 %CI) 11.08 (6.98–17.59); p < 0.00001). In addition, SLE patients also exhibited an increase in the left atrial diameter (LAD) (WMD—weighted mean difference (95 %CI) 0.18 (0.06–0.29); p = 0.002), the left ventricular internal diameter in diastole (LVDd) (WMD (95 %CI) 0.07 (0.02–0.12); p = 0.01), and the left ventricular mass index (LVMI) (WMD (95 %CI) 5.69 (2.69–8.69); p = 0.0002). In contrast, the left ventricular systolic function (WMD (95 %CI) −1.22 (−1.69 to −0.75); p < 0.00001) and diastolic function including E/A ratio and E/E’ ratio (WMD (95  % CI) −0.13 (−0.24 to −0.01); p = 0.04; WMD (95  % CI) 1.71 (0.43 to 2.99); p = 0.009) were decreased in SLE patients. Patients with SLE are associated with significant alterations in cardiac structure and function as demonstrated by echocardiography. Data from this study suggest that echocardiographic assessment should be considered as a part of routine examinations for SLE patients clinically.


Cardiac structure and function Echocardiography Systemic lupus erythematosus Systemic review and meta-analysis 



We would like to thank Professor Hui Y. Lan for his expert assistance in the manuscript editing. This study is supported by a grant from the Guangdong Natural Science Foundation (S2012010009667).

Compliance with ethical standards




  1. 1.
    Mok CC (2011) Epidemiology and survival of systemic lupus erythematosus in Hong Kong Chinese. Lupus 20:767–771CrossRefPubMedGoogle Scholar
  2. 2.
    Urowitz MB, Bookman AA, Koehler BE, et al. (1976) The bimodal mortality pattern of systemic lupus erythematosus. Am J Med 60:221–225CrossRefPubMedGoogle Scholar
  3. 3.
    Doria A, Iaccarino L, Ghirardello A, et al. (2006) Long-term prognosis and causes of death in systemic lupus erythematosus. Am J Med 119:700–706CrossRefPubMedGoogle Scholar
  4. 4.
    Gustafsson JT, Simard JF, Gunnarsson I, et al. (2012) Risk factors for cardiovascular mortality in patients with systemic lupus erythematosus, a prospective cohort study. Arthritis Res Ther 14:46CrossRefGoogle Scholar
  5. 5.
    Chen SC, Chang JM, Liu WC, et al. (2012) Echocardiographic parameters are independently associated with increased cardiovascular events in patients with chronic kidney disease. Nephrol Dial Transplant 27:1064–1070CrossRefPubMedGoogle Scholar
  6. 6.
    Doria A, Iaccarino L, Sarzi-Puttini P, et al. (2005) Cardiac involvement in systemic lupus erythematosus. Lupus 14:683–686CrossRefPubMedGoogle Scholar
  7. 7.
    Wislowska M, Deren D, Kochmanski M, et al. (2009) Systolic and diastolic heart function in SLE patients. Rheumatol Int 29:1469–1476CrossRefPubMedGoogle Scholar
  8. 8.
    Gin PL, Wang WC, Yang SH, et al. (2006) Right heart function in systemic lupus erythematosus: insights from myocardial Doppler tissue imaging. J Am Soc Echocardiogr 19:441–449CrossRefPubMedGoogle Scholar
  9. 9.
    Roman MJ, Salmon JE, Sobel R, et al. (2001) Prevalence and relation to risk factors of carotid atherosclerosis and left ventricular hypertrophy in systemic lupus erythematosus and antiphospholipid antibody syndrome. Am J Cardiol 87:663–666CrossRefPubMedGoogle Scholar
  10. 10.
    Shang Q, Yip GW, Tam LS, et al. (2012) SLICC/ACR damage index independently associated with left ventricular diastolic dysfunction in patients with systemic lupus erythematosus. Lupus 21:1057–1062CrossRefPubMedGoogle Scholar
  11. 11.
    Gabrielli F, Alcini E, Prima MA, et al. (1996) Cardiac involvement in connective tissue diseases and primary antiphospholipid syndrome: echocardiographic assessment and correlation with antiphospholipid antibodies. Acta Cardiol 51:425–439PubMedGoogle Scholar
  12. 12.
    Leszczynski P, Straburzynska-Migaj E, Korczowska I, et al. (2003) Cardiac valvular disease in patients with systemic lupus erythematosus. Relationship with anticardiolipin antibodies. Clin Rheumatol 22:405–408CrossRefPubMedGoogle Scholar
  13. 13.
    Jensen-Urstad K, Svenungsson E, de Faire U, et al. (2002) Cardiac valvular abnormalities are frequent in systemic lupus erythematosus patients with manifest arterial disease. Lupus 11:744–752CrossRefPubMedGoogle Scholar
  14. 14.
    Roldan CA, Shively BK, Crawford MH (1996) An echocardiographic study of valvular heart disease associated with systemic lupus erythematosus. N Engl J Med 335:1424–1430CrossRefPubMedGoogle Scholar
  15. 15.
    Plazak W, Kopec G, Tomkiewicz-Pajak L, et al. (2011) Heart structure and function in patients with generalized autoimmune diseases: echocardiography with tissue Doppler study. Acta Cardiol 66:159–165PubMedGoogle Scholar
  16. 16.
    Gabrielli F, Alcini E, Di Prima MA, et al. (1995) Cardiac valve involvement in systemic lupus erythematosus and primary antiphospholipid syndrome: lack of correlation with antiphospholipid antibodies. Int J Cardiol 51:117–126CrossRefPubMedGoogle Scholar
  17. 17.
    Roldan CA, Qualls CR, Sopko KS, et al. (2008) Transthoracic versus transesophageal echocardiography for detection of Libman-sacks endocarditis: a randomized controlled study. J Rheumatol 35:224–229PubMedGoogle Scholar
  18. 18.
    Paradiso M, Gabrielli F, Masala C, et al. (2001) Evaluation of myocardial involvement in systemic lupus erythematosus by signal-averaged electrocardiography and echocardiography. Acta Cardiol 56:381–386CrossRefPubMedGoogle Scholar
  19. 19.
    Teixeira AC, Bonfa E, Herskowictz N, et al. (2010) Early detection of global and regional left ventricular diastolic dysfunction in systemic lupus erythematosus: the role of the echocardiography. Rev Bras Rheumatol 50:16–30CrossRefGoogle Scholar
  20. 20.
    Amoroso A, Cacciapaglia F, De Castro S, et al. (2006) The adjunctive role of antiphospholipid antibodies in systemic lupus erythematosus cardiac involvement. Clin Exp Rheumatol 24:287–294PubMedGoogle Scholar
  21. 21.
    Toumanidis ST, Papamichael CM, Antoniades LG, et al. (1995) Cardiac involvement in collagen diseases. Eur Heart J 16:257–262PubMedGoogle Scholar
  22. 22.
    Falcao CA, Alves IC, Chahade WH, et al. (2002) Echocardiographic abnormalities and antiphospholipid antibodies in patients with systemic lupus erythematosus. Arq Bras Cardiol 79:285–291CrossRefPubMedGoogle Scholar
  23. 23.
    Wranicz JK, Cygankiewicz I, Zielinska M, et al. (2001) Non-invasive cardiac evaluation in patients with systemic lupus erythematosus. J Med 32:195–206PubMedGoogle Scholar
  24. 24.
    Lee SW, Park MC, Park YB, et al. (2008) E/E’ ratio is more sensitive than E/a ratio for detection of left ventricular diastolic dysfunction in systemic lupus erythematosus. Lupus 17:195–201CrossRefPubMedGoogle Scholar
  25. 25.
    Perez-Villa F, Font J, Azqueta M, et al. (2005) Severe valvular regurgitation and antiphospholipid antibodies in systemic lupus erythematosus: a prospective, long-term, follow up study. Arthritis Rheum 53:460–467CrossRefPubMedGoogle Scholar
  26. 26.
    Kalke S, Balakrishanan C, Mangat G, et al. (1998) Echocardiography in systemic lupus erythematosus. Lupus 7:540–544CrossRefPubMedGoogle Scholar
  27. 27.
    Cervera R, Font J, Pare C, et al. (1992) Cardiac disease in systemic lupus erythematosus: prospective study of 70 patients. Ann Rheum Dis 51:156–159CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Yu XH, Li YN (2011) Echocardiographic abnormalities in a cohort of Chinese patients with systemic lupus erythematosus—a retrospective analysis of eighty-five cases. J Clin Ultrasound 39:519–526CrossRefPubMedGoogle Scholar
  29. 29.
    Pocock SJ, Collier TJ, Dandreo KJ, et al. (2004) Issues in the reporting of epidemiological studies: a survey of recent practice. BMJ 329:883CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Stroup DF, Berlin JA, Morton SC, et al. (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA 283:2008–2012CrossRefPubMedGoogle Scholar
  31. 31.
    Phillips B, Ball C, Sackett D (2012) Levels of evidence and grades of recommendation. Oxford Centre for Evidence-based Medicine Web site.
  32. 32.
    Wells GA, Shea B, O’Connell D et al (2012) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Ottawa Hospital Research Institute Web site.
  33. 33.
    Higgins JP, Thompson SG (2008) Cochrane handbook for systematic reviews of interventions. Cochrane Collaboration, New YorkCrossRefGoogle Scholar
  34. 34.
    Maksimovic R, Seferovic PM, Ristic AD, et al. (2006) Cardiac imaging in rheumatic diseases. Rheumatology (Oxford) 45(Suppl 4):v26–v31Google Scholar
  35. 35.
    Sugiura T, Kumon Y, Kataoka H, et al. (2009) Asymptomatic pericardial effusion in patients with systemic lupus erythematosus. Lupus 18:128–132CrossRefPubMedGoogle Scholar
  36. 36.
    Omdal R, Lunde P, Rasmussen K, et al. (2001) Transesophageal and transthoracic echocardiography and Doppler-examinations in systemic lupus erythematosus. Scand J Rheumatol 30:275–281CrossRefPubMedGoogle Scholar
  37. 37.
    Bidani AK, Roberts JL, Schwartz MM, et al. (1980) Immunopathology of cardiac lesions in fatal systemic lupus erythematosus. Am J Med 69:849–858CrossRefPubMedGoogle Scholar
  38. 38.
    Crozier IG, Li E, Milne MJ, et al. (1990) Cardiac involvement in systemic lupus erythematosus detected by echocardiography. Am J Cardiol 65:1145–1148CrossRefPubMedGoogle Scholar
  39. 39.
    Pieretti J, Roman MJ, Devereux RB, et al. (2007) Systemic lupus erythematosus predicts increased left ventricular mass. Circulation 116:419–426CrossRefPubMedGoogle Scholar
  40. 40.
    Yip GW, Shang Q, Tam LS, et al. (2009) Disease chronicity and activity predict subclinical left ventricular systolic dysfunction in patients with systemic lupus erythematosus. Heart 95:980–987CrossRefPubMedGoogle Scholar
  41. 41.
    Paran D, Caspi D, Levartovsky D, et al. (2007) Cardiac dysfunction in patients with systemic lupus erythematosus and antiphospholipid syndrome. Ann Rheum Dis 66:506–510CrossRefPubMedGoogle Scholar
  42. 42.
    Tincani A, Rebaioli CB, Taglietti M, et al. (2006) Heart involvement in systemic lupus erythematosus, anti-phospholipid syndrome and neonatal lupus. Rheumatology (Oxford) 45(Suppl 4):v8–v13Google Scholar
  43. 43.
    Mavrogeni S, Bratis K, Kolovou G (2012) Pathophysiology of Q waves in II, III, avF in systemic lupus erythematosus. Evaluation using cardiovascular magnetic resonance imaging. Lupus 21:821–829CrossRefPubMedGoogle Scholar
  44. 44.
    Ishimori ML, Martin R, Berman DS, et al. (2011) Myocardial ischemia in the absence of obstructive coronary artery disease in systemic lupus erythematosus. JACC Cardiovasc Imaging 4:27–33CrossRefPubMedGoogle Scholar
  45. 45.
    Mavrogeni S, Dimitroulas T, Kitas GD (2012) Multimodality imaging and the emerging role of cardiac magnetic resonance in autoimmune myocarditis. Autoimmun Rev 12:305–312CrossRefPubMedGoogle Scholar
  46. 46.
    Mavrogeni S, Vassilopoulos D (2011) Is there a place for cardiovascular magnetic resonance imaging in the evaluation of cardiovascular involvement in rheumatic diseases? Semin Arthritis Rheum 41:488–496CrossRefPubMedGoogle Scholar
  47. 47.
    Deetjen AG, Conradi G, Mollmann S, et al. (2007) Diagnostic value of the 16-detector row multislice spiral computed tomography for the detection of coronary artery stenosis in comparison to invasive coronary angiography. Clin Cardiol 30:118–123CrossRefPubMedGoogle Scholar
  48. 48.
    George SM, Kalantarinia K (2011) The role of imaging in the management of cardiorenal syndrome. Int J Nephrol 2011:245241CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Hasebroock KM, Serkova NJ (2009) Toxicity of MRI and CT contrast agents. Expert Opin Drug Metab Toxicol 5:403–416CrossRefPubMedGoogle Scholar
  50. 50.
    Pennell DJ, Sechtem UP, Higgins CB, et al. (2004) Clinical indications for cardiovascular magnetic resonance (CMR): consensus panel report. J Cardiovasc Magn Reson 6:727–765CrossRefPubMedGoogle Scholar

Copyright information

© International League of Associations for Rheumatology (ILAR) 2016

Authors and Affiliations

  • Junzhe Chen
    • 1
  • Ying Tang
    • 1
  • Mingsheng Zhu
    • 1
  • Anping Xu
    • 1
    Email author
  1. 1.Department of Nephrology, Sun Yat-sen Memorial HospitalSun Yat-sen UniversityGuangzhouChina

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