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Pulmonary hypertension in systemic lupus erythematosus: an independent predictor of patient survival

  • Min, Hong Ki (Division of Rheumatology, Department of Internal Medicine, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Lee, Jae Ho (Division of Rheumatology, Department of Internal Medicine, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Jung, Seung Min (Division of Rheumatology, Department of Internal Medicine, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Lee, Jennifer (Division of Rheumatology, Department of Internal Medicine, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Kang, Kwi Young (Division of Rheumatology, Department of Internal Medicine, Incheon St. Mary's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Kwok, Seung-Ki (Division of Rheumatology, Department of Internal Medicine, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Ju, Ji Hyeon (Division of Rheumatology, Department of Internal Medicine, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Park, Kyung-Su (Division of Rheumatology, Department of Internal Medicine, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Park, Sung-Hwan (Division of Rheumatology, Department of Internal Medicine, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea)
  • Received : 2014.03.01
  • Accepted : 2014.04.01
  • Published : 2015.03.01

Abstract

Background/Aims: We investigated whether transthoracic echocardiographysuspected pulmonary hypertension (PH) affects survival in systemic lupus erythematosus (SLE) patients and examined factors associated with PH occurrence and survival. Methods: This retrospective single-center study included 154 Korean SLE patients fulfilling the American College of Rheumatology criteria (January 1995 to June 2013). Student t test, Mann-Whitney U test, Kaplan-Meier curves, and log-rank tests were used for comparisons. Results: A total of 35 SLE patients with PH (SLE/PH+) and 119 without PH (SLE/PH-) were analyzed. Higher percentages of interstitial lung disease, Raynaud's phenomenon (RP), World Health Organization functional classification III/IV, and cardiomegaly were found in SLE/PH+ compared to SLE/PH-. Furthermore, the Systemic Lupus International Collaborating Clinics/American College of Rheumatology Damage Index was significantly higher in SLE/PH+ ($2.46{\pm}1.245$ vs. $1.00{\pm}1.235$), whereas survival rates were significantly higher in SLE/PH- in log-rank tests (p = 0.001). In multivariate analysis, the adjusted mortality hazard ratio (HR) for SLE/PH+ patients was 3.10. Subgroup analysis demonstrated a higher percentage of lupus nephritis in the SLE/PH+ patients who died (p = 0.039) and low complement-3 levels (p = 0.007). In univariate analysis, the mortality HR for SLE/PH+ patients with lupus nephritis was 4.62, whereas the presence of RP decreased the mortality risk in multivariate analysis; adjusted HR, 0.10. Conclusions: PH is an independent factor predicting survival in SLE patients. The presence of lupus nephritis resulted in an increased trend for mortality, whereas coexistence of RP was associated with a better survival prognosis in SLE/PH+ patients.

Keywords

References

  1. Perez HD, Kramer N. Pulmonary hypertension in systemic lupus erythematosus: report of four cases and review of the literature. Semin Arthritis Rheum 1981;11:177-181. https://doi.org/10.1016/0049-0172(81)90098-6
  2. Simonson JS, Schiller NB, Petri M, Hellmann DB. Pulmonary hypertension in systemic lupus erythematosus. J Rheumatol 1989;16:918-925.
  3. Asherson RA, Higenbottam TW, Dinh Xuan AT, Khamashta MA, Hughes GR. Pulmonary hypertension in a lupus clinic: experience with twenty-four patients. J Rheumatol 1990;17:1292-1298.
  4. Winslow TM, Ossipov MA, Fazio GP, Simonson JS, Redberg RF, Schiller NB. Five-year follow-up study of the prevalence and progression of pulmonary hypertension in systemic lupus erythematosus. Am Heart J 1995;129:510-515. https://doi.org/10.1016/0002-8703(95)90278-3
  5. Li EK, Tam LS. Pulmonary hypertension in systemic lupus erythematosus: clinical association and survival in 18 patients. J Rheumatol 1999;26:1923-1929.
  6. Pan TL, Thumboo J, Boey ML. Primary and secondary pulmonary hypertension in systemic lupus erythematosus. Lupus 2000;9:338-342. https://doi.org/10.1191/096120300678828361
  7. Tanaka E, Harigai M, Tanaka M, Kawaguchi Y, Hara M, Kamatani N. Pulmonary hypertension in systemic lupus erythematosus: evaluation of clinical characteristics and response to immunosuppressive treatment. J Rheumatol 2002;29:282-287.
  8. Johnson SR, Gladman DD, Urowitz MB, Ibanez D, Granton JT. Pulmonary hypertension in systemic lupus. Lupus 2004;13:506-509. https://doi.org/10.1191/0961203303lu1051oa
  9. Cefle A, Inanc M, Sayarlioglu M, et al. Pulmonary hypertension in systemic lupus erythematosus: relationship with antiphospholipid antibodies and severe disease outcome. Rheumatol Int 2011;31:183-189. https://doi.org/10.1007/s00296-009-1255-2
  10. Funauchi M, Shimadzu H, Tamaki C, et al. Survival study by organ disorders in 306 Japanese patients with systemic lupus erythematosus: results from a single center. Rheumatol Int 2007;27:243-249.
  11. 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.
  12. Kang KY, Kwok SK, Ju JH, et al. The causes of death in Korean patients with systemic lupus erythematosus over 11 years. Lupus 2011;20:989-997. https://doi.org/10.1177/0961203311402245
  13. Lian F, Chen D, Wang Y, et al. Clinical features and independent predictors of pulmonary arterial hypertension in systemic lupus erythematosus. Rheumatol Int 2012;32:1727-1731. https://doi.org/10.1007/s00296-011-1880-4
  14. Xia YK, Tu SH, Hu YH, et al. Pulmonary hypertension in systemic lupus erythematosus: a systematic review and analysis of 642 cases in Chinese population. Rheumatol Int 2013;33:1211-1217. https://doi.org/10.1007/s00296-012-2525-y
  15. Tan EM, Cohen AS, Fries JF, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982;25:1271-1277. https://doi.org/10.1002/art.1780251101
  16. Ruiz-Irastorza G, Garmendia M, Villar I, Egurbide MV, Aguirre C. Pulmonary hypertension in systemic lupus erythematosus: prevalence, predictors and diagnostic strategy. Autoimmun Rev 2013;12:410-415. https://doi.org/10.1016/j.autrev.2012.07.010
  17. Kim KJ, Baek IW, Park YJ, Yoon CH, Kim WU, Cho CS. High levels of uric acid in systemic lupus erythematosus is associated with pulmonary hypertension. Int J Rheum Dis 2014 Jan 16 [Epub]. http://dx.doi.org/ 10.1111/1756-185X.12262.
  18. Rosenkranz S. Pulmonary hypertension: current diagnosis and treatment. Clin Res Cardiol 2007;96:527-541. https://doi.org/10.1007/s00392-007-0526-8
  19. Chung SM, Lee CK, Lee EY, Yoo B, Lee SD, Moon HB. Clinical aspects of pulmonary hypertension in patients with systemic lupus erythematosus and in patients with idiopathic pulmonary arterial hypertension. Clin Rheumatol 2006;25:866-872. https://doi.org/10.1007/s10067-006-0206-5
  20. Galie N, Hoeper MM, Humbert M, et al. Guidelines for the diagnosis and treatment of pulmonary hypertension: the Task Force for the Diagnosis and Treatment of Pulmonary Hypertension of the European Society of Cardiology (ESC) and the European Respiratory Society (ERS), endorsed by the International Society of Heart and Lung Transplantation (ISHLT). Eur Heart J 2009;30:2493-2537. https://doi.org/10.1093/eurheartj/ehp297
  21. Chow SL, Chandran V, Fazelzad R, Johnson SR. Prognostic factors for survival in systemic lupus erythematosus associated pulmonary hypertension. Lupus 2012;21:353-364. https://doi.org/10.1177/0961203311429815
  22. Prabu A, Patel K, Yee CS, et al. Prevalence and risk factors for pulmonary arterial hypertension in patients with lupus. Rheumatology (Oxford) 2009;48:1506-1511. https://doi.org/10.1093/rheumatology/kep203
  23. Fois E, Le Guern V, Dupuy A, Humbert M, Mouthon L, Guillevin L. Noninvasive assessment of systolic pulmonary artery pressure in systemic lupus erythematosus: retrospective analysis of 93 patients. Clin Exp Rheumatol 2010;28:836-841.

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