Journal List > J Rheum Dis > v.21(2) > 1064163

J Rheum Dis. 2014 Apr;21(2):54-63. Korean.
Published online April 30, 2014.
Copyright © 2014 by The Korean College of Rheumatology
The Present and Future of Clinical Research for Korean Lupus Patients
Dam Kim, Soo-Kyung Cho and Yoon-Kyoung Sung
Department of Rheumatology, Hanyang University Hospital for Rheumatic Diseases, Seoul, Korea.

Corresponding to: Yoon-Kyoung Sung, Department of Rheumatology, Hanyang University Hospital for Rheumatic Diseases, Wangsimni-ro, Seongdong-gu, Seoul 133-792, Korea. Email:
Received April 09, 2014; Revised April 24, 2014; Accepted April 25, 2014.

This is a Free Access article, which permits unrestricted non-commerical use, distribution, and reproduction in any medium, provided the original work is properly cited.


Systemic lupus erythematosus (SLE) is considered to be the prototype of systemic autoimmune disease because it involves the most immune cells and it can affect all organs of the human body. Despite the advances in understanding the etiology and pathogenesis of SLE, a sobering fact is that only a few drugs have been licensed for its treatment. This may be associated with the difficulties in performing clinical trials due to its diverse clinical manifestations and comorbidities of SLE, as well as difficulties in determining the disease outcome. To determine the natural course and drug response of SLE patients, various observational studies have been conducted in Western countries. However, in Korea, sufficiently powered prospective clinical studies are scarce. In this review, we conducted a systematic review to be aware of the current status of clinical studies in Korean SLE patients. Identifying the topics for clinical studies that have been performed helps determine how the clinical research should be conducted for Korean SLE patients.

Keywords: Lupus erythematosus; Systemic; Clinical study; Korean


Figure 1
Selection of studies included in this review of systemic lupus erythematosus clinical researches.
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Table 1
Summary of the studies about lupus nephritis clinical researches in Korea
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Table 2
Summary of the studies about lupus outcome clinical researches in Korea
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Table 3
Summary of the studies about lupus comorbidity clinical researches in Korea
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1. D'Cruz DP, Khamashta MA, Hughes GR. Systemic lupus erythematosus. Lancet 2007;369:587–596.
2. Shim JS, Sung YK, Joo YB, Lee HS, Bae SC. Prevalence and incidence of systemic lupus erythematosus in South Korea. Rheumatol Int. 2013
[Epub ahead of print].
3. Merrell M, Shulman LE. Determination of prognosis in chronic disease, illustrated by systemic lupus erythematosus. J Chronic Dis 1955;1:12–32.
4. Pons-Estel GJ, Alarcón GS, Scofield L, Reinlib L, Cooper GS. Understanding the epidemiology and progression of systemic lupus erythematosus. Semin Arthritis Rheum 2010;39:257–268.
5. Bongu A, Chang E, Ramsey-Goldman R. Can morbidity and mortality of SLE be improved. Best Pract Res Clin Rheumatol 2002;16:313–332.
6. Lau CS, Mak A. The socioeconomic burden of SLE. Nat Rev Rheumatol 2009;5:400–404.
7. Slawsky KA, Fernandes AW, Fusfeld L, Manzi S, Goss TF. A structured literature review of the direct costs of adult systemic lupus erythematosus in the US. Arthritis Care Res (Hoboken) 2011;63:1224–1232.
8. Saxena R, Mahajan T, Mohan C. Lupus nephritis: current update. Arthritis Res Ther 2011;13:240.
9. Youm JY, Sung YK, Uhm WS, Jun JB, Yoo DH, Bae SC. Rituximab Treatment for the Patient with Refractory Lupus Nephritis. J Korean Rheum Assoc 2005;12:251–262.
10. Lee T, Oh KH, Joo KW, Kim YS, Ahn C, Han JS, et al. Tacrolimus is an alternative therapeutic option for the treatment of refractory lupus nephritis. Lupus 2010;19:974–980.
11. Seong SS, Choi CB, Yun HR, Kim YJ, Sung YK, Bae SC. Effect of lower dose intravenous cyclophosphamide on remission induction in Korean patients with lupus nephritis. Rheumatol Int 2008;28:453–458.
12. Koo HS, Kim YC, Lee SW, Kim DK, Oh KH, Joo KW, et al. The effects of cyclophosphamide and mycophenolate on end-stage renal disease and death of lupus nephritis. Lupus 2011;20:1442–1449.
13. So MW, Koo BS, Kim YG, Lee CK, Yoo B. Predictive value of remission status after 6 months induction therapy in patients with proliferative lupus nephritis: a retrospective analysis. Clin Rheumatol 2011;30:1399–1405.
14. Moon SJ, Park HS, Kwok SK, Ju J, Choi BS, Park KS, et al. Predictors of renal relapse in Korean patients with lupus nephritis who achieved remission six months following induction therapy. Lupus 2013;22:527–537.
15. Kang SH, Chung BH, Choi SR, Lee JY, Park HS, Sun IO, et al. Comparison of clinical outcomes by different renal replacement therapy in patients with end-stage renal disease secondary to lupus nephritis. Korean J Intern Med 2011;26:60–67.
16. Park MC, Park YB, Jung SY, Chung IH, Choi KH, Lee SK. Risk of ovarian failure and pregnancy outcome in patients with lupus nephritis treated with intravenous cyclophosphamide pulse therapy. Lupus 2004;13:569–574.
17. Lee SG, Cho YM, So MW, Kim SS, Kim YG, Lee CK, et al. ISN/RPS 2003 class II mesangial proliferative lupus nephritis: a comparison between cases that progressed to class III or IV and cases that did not. Rheumatol Int 2012;32:2459–2464.
18. You SJ, Park JS, Kim JH, Park SK, Bae SC, Kim GH, et al. Clinicopathological Correlation of Lupus Nephritis. Korean J Nephrol 2009;28:410–417.
19. Kim JE, Hwang EA, Yoon JS, Jang MH, Kim SH, Han SY, et al. Treatment of Lupus Nephritis: A 21 Year, Single Center Experience. Korean J Nephrol 2009;28:113–121.
20. Moon SJ, Kim DK, Park SY, Chang JH, Kim HW, Lee JE, et al. A comparison study between mycophenolate mofetil and cyclophosphamide for treatment of proliferative lupus nephritis. Korean J Med 2008;74:640–647.
21. Kim YG, Kim HW, Cho YM, Oh JS, Nah SS, Lee CK, et al. The difference between lupus nephritis class IV-G and IV-S in Koreans: focus on the response to cyclophosphamide induction treatment. Rheumatology (Oxford) 2008;47:311–314.
22. Goo YS, Park HC, Choi HY, Kim BS, Park YB, Lee SK, et al. The evolution of lupus activity among patients with end-stage renal disease secondary to lupus nephritis. Yonsei Med J 2004;45:199–206.
23. Yoo CW, Kim MK, Lee HS. Predictors of renal outcome in diffuse proliferative lupus nephropathy: data from repeat renal biopsy. Nephrol Dial Transplant 2000;15:1604–1608.
24. Chin HJ, Kim SG. The Clinicopathologic Findings and Prognostic Factors Related to Death of Patients with Lupus Nephritis. Korean J Nephrol 2000;19:1129–1142.
25. Boumpas DT, Austin HA 3rd, Vaughn EM, Klippel JH, Steinberg AD, Yarboro CH, et al. Controlled trial of pulse methylprednisolone versus two regimens of pulse cyclophosphamide in severe lupus nephritis. Lancet 1992;340:741–745.
26. Houssiau FA, Vasconcelos C, DCruz D, Sebastiani GD, Garrido Ed, Danieli MG, et al. Immunosuppressive therapy in lupus nephritis: the Euro-Lupus Nephritis Trial, a randomized trial of low-dose versus high-dose intravenous cyclophosphamide. Arthritis Rheum 2002;46:2121–2131.
27. Appel GB, Contreras G, Dooley MA, Ginzler EM, Isenberg D, Jayne D, et al. Mycophenolate mofetil versus cyclophosphamide for induction treatment of lupus nephritis. J Am Soc Nephrol 2009;20:1103–1112.
28. Chan TM, Tse KC, Tang CS, Mok MY, Li FK. Hong Kong Nephrology Study Group. Long-term study of mycophenolate mofetil as continuous induction and maintenance treatment for diffuse proliferative lupus nephritis. J Am Soc Nephrol 2005;16:1076–1084.
29. Kang KY, Kwok SK, Ju JH, Park KS, Cho CS, Kim HY, et al. The causes of death in Korean patients with systemic lupus erythematosus over 11 years. Lupus 2011;20:989–997.
30. Kang KY, Kim HO, Yoon HS, Lee J, Lee WC, Ko HJ, et al. Incidence of cancer among female patients with systemic lupus erythematosus in Korea. Clin Rheumatol 2010;29:381–388.
31. Chun JH, Shin KC, Park CW, Doh GS, Lee CK, Hyun MS, et al. Clinical Manifestations On Systemic Lupus Erythematosus. J Korean Rheum Assoc 1994;1:159–168.
32. Chun BC, Bae SC. Mortality and cancer incidence in Korean patients with systemic lupus erythematosus: results from the Hanyang lupus cohort in Seoul, Korea. Lupus 2005;14:635–638.
33. Sung YK, Hur NW, Sinskey JL, Park D, Bae SC. Assessment of damage in Korean patients with systemic lupus erythematosus. J Rheumatol 2007;34:987–991.
34. Sung YK, Oh KT, Kwak EJ, Lee HS, Kim TH, Jun JB, et al. Health-Related Quality of Life in Korean Patients with Systemic Lupus Erythematosus. J Korean Rheum Assoc 2002;9 Suppl:S84–S95.
35. Yurkovich M, Vostretsova K, Chen W, Aviña-Zubieta JA. Overall and cause-specific mortality in patients with systemic lupus erythematosus: a meta-analysis of observational studies. Arthritis Care Res (Hoboken) 2014;66:608–616.
36. Ni J, Qiu LJ, Hu LF, Cen H, Zhang M, Wen PF, et al. Lung, liver, prostate, bladder malignancies risk in systemic lupus erythematosus: evidence from a meta-analysis. Lupus 2014;23:284–292.
37. Gladman D, Ginzler E, Goldsmith C, Fortin P, Liang M, Urowitz M, et al. Systemic lupus international collaborative clinics: development of a damage index in systemic lupus erythematosus. J Rheumatol 1992;19:1820–1821.
38. Kim SY, Lee JH. Prognosis of neonates in pregnant women with systemic lupus erythematosus. Yonsei Med J 2008;49:515–520.
39. Kang HS, Song SE, Ma JS, Choi YY, Song TB. The Clinical Characteristics and Outcome of Neonates born to Systemic Lupus Erythematosus Mothers. J Korean Soc Neonatol 2006;13:139–148.
40. Baek HS, Choi JH, Kim NS, Kim CR, Moon SJ. Outcome of pregnant mothers with systemic lupus erythematosus (focusing on congenital heart block). Korean J Pediatr 2006;49:381–387.
41. Kim WU, Min JK, Kwun NK, Park SH, Hong YS, Lee SH, et al. Obstetric Outcomes in Patients with Systemic Lupus Erythematosus. J Korean Rheum Assoc 1997;4:131–138.
42. Shin JH, Lee EY, Lee CK, Cho YS, Kim A, Yoo B, et al. Fetal outcome and clinical feature during pregnancy in systemic lupus erythematosus. Korean J Med 2003;65:511–519.
43. Ko HS, Ahn HY, Jang DG, Choi SK, Park YG, Park IY, et al. Pregnancy outcomes and appropriate timing of pregnancy in 183 pregnancies in Korean patients with SLE. Int J Med Sci 2011;8:577–583.
44. Lee CK, Ahn MS, Lee EY, Shin JH, Cho YS, Ha HK, et al. Acute abdominal pain in systemic lupus erythematosus: focus on lupus enteritis (gastrointestinal vasculitis). Ann Rheum Dis 2002;61:547–550.
45. Kim WU, Kim SI, Yoo WH, Park JH, Min JK, Kim SC, et al. Adult respiratory distress syndrome in systemic lupus erythematosus: causes and prognostic factors: a single center, retrospective study. Lupus 1999;8:552–557.
46. Kim JM, Kwok SK, Ju JH, Kim HY, Park SH. Idiopathic intracranial hypertension as a significant cause of intractable headache in patients with systemic lupus erythematosus: a 15-year experience. Lupus 2012;21:542–547.
47. Oh DH, Kim SH, Jung S, Sung YK, Bang SY, Bae SC, et al. Precuneus hypoperfusion plays an important role in memory impairment of patients with systemic lupus erythematosus. Lupus 2011;20:855–860.
48. Lee CH, Lee JS, Song CH, Lee SK. Clinical Evaluation of Neuropsychiatric Lupus Erythematosus. J Korean Rheum Assoc 1996;3:126–133.
49. Cho BS, Kim HS, Oh SJ, Koh HJ, Yoon CH, Jung SL, et al. Comparison of the clinical manifestations, brain MRI and prognosis between neuroBeçhet's disease and neuropsychiatric lupus. Korean J Intern Med 2007;22:77–86.
50. Kim JM, Kim KJ, Yoon HS, Kwok SK, Ju JH, Park KS, et al. Meningitis in Korean patients with systemic lupus erythematosus: analysis of demographics, clinical features and outcomes; experience from affiliated hospitals of the Catholic University of Korea. Lupus 2011;20:531–536.
51. Lim MK, Suh CH, Kim HJ, Cho YK, Choi SH, Kang JH, et al. Systemic lupus erythematosus: brain MR imaging and single-voxel hydrogen 1 MR spectroscopy. Radiology 2000;217:43–49.
52. Jung SM, Moon SJ, Kwok SK, Ju JH, Park KS, Park SH, et al. Posterior reversible encephalopathy syndrome in Korean patients with systemic lupus erythematosus: risk factors and clinical outcome. Lupus 2013;22:885–891.
53. Kim HJ, Park YJ, Kim WU, Park SH, Cho CS. Invasive fungal infections in patients with systemic lupus erythematosus: experience from affiliated hospitals of Catholic University of Korea. Lupus 2009;18:661–666.
54. Yun JE, Lee SW, Kim TH, Jun JB, Jung S, Bae SC, et al. The incidence and clinical characteristics of Mycobacterium tuberculosis infection among systemic lupus erythematosus and rheumatoid arthritis patients in Korea. Clin Exp Rheumatol 2002;20:127–132.
55. Kwok SK, Moon SJ, Ju JH, Park KS, Kim WU, Cho CS, et al. Diffuse alveolar hemorrhage in systemic lupus erythematosus: risk factors and clinical outcome: results from affiliated hospitals of Catholic University of Korea. Lupus 2011;20:102–107.
56. Her M, Lee Y, Jung E, Kim T, Kim D. Liver enzyme abnormalities in systemic lupus erythematosus: a focus on toxic hepatitis. Rheumatol Int 2011;31:79–84.
57. Oh SN, Jee WH, Cho SM, Kim SH, Kang HS, Ryu KN, et al. Osteonecrosis in patients with systemic lupus erythematosus: MR imaging and scintigraphic evaluation. Clin Imaging 2004;28:305–309.
58. Bae YI, Yun SJ, Lee JB, Kim SJ, Won YH, Lee SC. A clinical and epidemiological study of lupus erythematosus at a tertiary referral dermatology clinic in Korea. Lupus 2009;18:1320–1326.
59. Kim BY, Kang MK, Ahn TJ, Lee TH, Choi JH. Otologic Manifestations in Patients with Systemic Lupus Erythematosus. Korean J Otorhinolaryngol-Head Neck Surg 2008;51:416–421.
60. Yun SJ, Lee JW, Yoon HJ, Lee SS, Kim SY, Lee JB, et al. Cross-sectional study of hair loss patterns in 122 Korean systemic lupus erythematosus patients: a frequent finding of non-scarring patch alopecia. J Dermatol 2007;34:451–455.
61. Ha Y, Lee KH, Jung S, Lee SW, Lee SK, Park YB. Glucocorticoid-induced diabetes mellitus in patients with systemic lupus erythematosus treated with high-dose glucocorticoid therapy. Lupus 2011;20:1027–1034.
62. González LA, Toloza SM, McGwin G Jr, Alarcón GS. Ethnicity in systemic lupus erythematosus (SLE): its influence on susceptibility and outcomes. Lupus 2013;22:1214–1224.
63. Mok CC, Yap DY, Navarra SV, Liu ZH, Zhao MH, Lu L, et al. Asian Lupus Nephritis Network (ALNN). Overview of lupus nephritis management guidelines and perspective from Asia. Int J Rheum Dis 2013;16:625–636.
64. Gatto M, Kiss E, Naparstek Y, Doria A. In-/off-label use of biologic therapy in systemic lupus erythematosus. BMC Med 2014;12:30.
65. ter Borg EJ, Horst G, Hummel EJ, Limburg PC, Kallenberg CG. Measurement of increases in anti-double-stranded DNA antibody levels as a predictor of disease exacerbation in systemic lupus erythematosus. A long-term, prospective study. Arthritis Rheum 1990;33:634–643.
66. Akhter E, Burlingame RW, Seaman AL, Magder L, Petri M. Anti-C1q antibodies have higher correlation with flares of lupus nephritis than other serum markers. Lupus 2011;20:1267–1274.
67. Su D, Liu R, Li X, Sun L. Possible novel biomarkers of organ involvement in systemic lupus erythematosus. Clin Rheumatol. 2014
[Epub ahead of print].
68. Lee SW, Park MC, Lee SK, Park YB. Adjusted neutropenia is associated with early serious infection in systemic lupus erythematosus. Mod Rheumatol 2013;23:509–515.
69. Bang SY, Lee CK, Kang YM, Kim HA, Suh CH, Chung WT, et al. Multicenter retrospective analysis of the effectiveness and safety of rituximab in korean patients with refractory systemic lupus erythematosus. Autoimmune Dis 2012;2012:565039.
70. Kim JM, Kwok SK, Ju JH, Kim HY, Park SH. Reactive hemophagocytic syndrome in adult Korean patients with systemic lupus erythematosus: a case-control study and literature review. J Rheumatol 2012;39:86–93.
71. Park YJ, Park BH, Min DJ, Kim WU. Risk Factors for Low Bone Mineral Density in Korean Patients with Systemic Lupus Erythematosus. J Rheum Dis 2011;18:19–25.
72. Lee YH, Choe JY, Park SH, Park YW, Lee SS, Kang YM, et al. Prevalence of human papilloma virus infections and cervical cytological abnormalities among Korean women with systemic lupus erythematosus. J Korean Med Sci 2010;25:1431–1437.
73. Woo KS, Kim KE, Kim JM, Han JY, Chung WT, Kim KH. Prevalence and clinical associations of lupus anticoagulant, anticardiolipin antibodies, and anti-beta2-glycoprotein I antibodies in patients with systemic lupus erythematosus. Korean J Lab Med 2010;30:38–44.
74. Yoon CK, Park JH, Yu HG. Retinopathy Associated With Systemic Lupus Erythematosus. J Korean Ophthalmol Soc 2009;50:1215–1220.
75. Jeong SJ, Choi H, Lee HS, Han SH, Chin BS, Baek JH, et al. Incidence and risk factors of infection in a single cohort of 110 adults with systemic lupus erythematosus. Scand J Infect Dis 2009;41:268–274.
76. Kwok SK, Ju JH, Cho CS, Kim HY, Park SH. Thrombotic thrombocytopenic purpura in systemic lupus erythematosus: risk factors and clinical outcome: a single centre study. Lupus 2009;18:16–21.
77. Oh KC, Byun WM, Jang HW, Kim KR. MR Manifestations of the Brain in Neuropsychiatric Systemic Lupus Erythematosus Patients. J Korean Radiol Soc 2008;58:1–7.
78. Kim YG, Lee CK, Byeon JS, Myung SJ, Oh JS, Nah SS, et al. Serum cholesterol in idiopathic and lupus-related protein-losing enteropathy. Lupus 2008;17:575–579.
79. Kwok SK, Seo SH, Ju JH, Park KS, Yoon CH, Kim WU, et al. Lupus enteritis: clinical characteristics, risk factor for relapse and association with anti-endothelial cell antibody. Lupus 2007;16:803–809.
80. Lim MK, Lee CK, Ju YS, Cho YS, Lee MS, Yoo B, et al. Serum ferritin as a serologic marker of activity in systemic lupus erythematosus. Rheumatol Int 2001;20:89–93.
81. Suh CH, Jeong YS, Park HC, Lee CH, Lee J, Song CH, et al. Risk factors for infection and role of C-reactive protein in Korean patients with systemic lupus erythematosus. Clin Exp Rheumatol 2001;19:191–194.
82. Kim HY, Im JG, Goo JM, Lee JK, Song JW, Kim SK. Pulmonary tuberculosis in patients with systematic lupus erythematosus. AJR Am J Roentgenol 1999;173:1639–1642.
83. Byun JY, Ha HK, Yu SY, Min JK, Park SH, Kim HY, et al. CT features of systemic lupus erythematosus in patients with acute abdominal pain: emphasis on ischemic bowel disease. Radiology 1999;211:203–209.
84. Yang HI, Choi BS, Park SH, Lee SH, Cho CS, Kim HY. The Avascular Necrosis of Bone in Sle. J Korean Rheum Assoc 1996;3:118–125.