Towards new avenues in the management of lupus glomerulonephritis

Nature Reviews Rheumatology

Volumn 12, Issue 4, 2016, Pages 221-234

  Mok, C C ^a  

^a TUEN MUN HOSPITAL   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

ABATACEPT; ATACICEPT; AZATHIOPRINE; BELIMUMAB; BIIB 023; BIOLOGICAL MARKER; CYCLOPHOSPHAMIDE; CYCLOSPORIN A; GLUCOCORTICOID; HYDROXYCHLOROQUINE; LAQUINIMOD; METHYLPREDNISOLONE; MONOCLONAL ANTIBODY; MYCOPHENOLATE MOFETIL; OCRELIZUMAB; PLACEBO; PREDNISOLONE; PREDNISONE; RITUXIMAB; TACROLIMUS; UNCLASSIFIED DRUG; BIOLOGICAL FACTOR; CALCINEURIN INHIBITOR; HYBRID PROTEIN; IMMUNOLOGIC FACTOR; MYCOPHENOLIC ACID; QUINOLONE DERIVATIVE; TACI RECEPTOR-IGG FC FRAGMENT FUSION PROTEIN; TNFSF12 PROTEIN, HUMAN; TUMOR NECROSIS FACTOR;

ALOPECIA; AMENORRHEA; ARTHRALGIA; CARDIOVASCULAR DISEASE; CHINESE; DIABETES MELLITUS; DIARRHEA; DISEASE EXACERBATION; DRUG DOSE REDUCTION; DRUG DOSE TITRATION; DRUG EFFICACY; DRUG MEGADOSE; DRUG TOLERABILITY; ETHNIC DIFFERENCE; ETHNIC GROUP; GASTROINTESTINAL SYMPTOM; GINGIVA HYPERTROPHY; HEMORRHAGIC CYSTITIS; HERPES ZOSTER; HUMAN; HYPERTENSION; HYPERTRICHOSIS; IMMUNOSUPPRESSIVE TREATMENT; INFECTION; LEG CRAMP; LEUKOPENIA; LOW DRUG DOSE; LUPUS ERYTHEMATOSUS NEPHRITIS; MAINTENANCE THERAPY; MENSTRUATION DISORDER; MORBIDITY; MORTALITY; NAUSEA; NEOPLASM; NONHUMAN; OVARY DISEASE; OVARY INSUFFICIENCY; PNEUMONIA; PRIORITY JOURNAL; REMISSION; REPRODUCTIVE TOXICITY; REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS; TREMOR; VOMITING; ANALOGS AND DERIVATIVES; IMMUNOLOGY; LUPUS NEPHRITIS; PERSONALIZED MEDICINE; URINE;

ABATACEPT; ANTIBODIES, MONOCLONAL; ANTIBODIES, MONOCLONAL, HUMANIZED; BIOLOGICAL FACTORS; BIOMARKERS; CALCINEURIN INHIBITORS; CYCLOPHOSPHAMIDE; HUMANS; IMMUNOLOGIC FACTORS; LUPUS NEPHRITIS; MYCOPHENOLIC ACID; PRECISION MEDICINE; QUINOLONES; RECOMBINANT FUSION PROTEINS; RITUXIMAB; TUMOR NECROSIS FACTORS;

EID: 84953238452     PISSN: 17594790     EISSN: 17594804     Source Type: Journal    
DOI: 10.1038/nrrheum.2015.174     Document Type: Review

References (117)

1. Mok, C. C. Understanding lupus nephritis: diagnosis, management, and treatment options. Int. J. Womens Health 4, 213-222 (2012).
2. Mok, C. C., Wong, R. W. & Lau, C. S. Lupus nephritis in Southern Chinese patients: clinicopathologic findings and long-term outcome. Am. J. Kidney Dis. 34, 315-323 (1999).
3. Mok, C. C. et al. Long-term outcome of diffuse proliferative lupus glomerulonephritis treated with cyclophosphamide. Am. J. Med. 119, 355.e25-333.e33 (2006).
4. Korbet, S. M., Schwartz, M. M., Evans, J. & Lewis, E. J. Severe lupus nephritis: racial differences in presentation and outcome. J. Am. Soc. Nephrol. 18, 244-254 (2007).
5. Hui, M. et al. Lupus nephritis: a 15-year multi-centre experience in the UK. Lupus 22, 328-332 (2013).
6. Mok, C. C., Kwok, R. C. & Yip, P. S. Effect of renal disease on the standardized mortality ratio and life expectancy of patients with systemic lupus erythematosus. Arthritis Rheum. 65, 2154-2160 (2013).
7. Fernández, M. et al. A multiethnic, multicenter cohort of patients with systemic lupus erythematosus (SLE) as a model for the study of ethnic disparities in SLE. Arthritis Rheum. 57, 576-584 (2007).
8. Sánchez, E. et al. Impact of genetic ancestry and sociodemographic status on the clinical expression of systemic lupus erythematosus in American Indian European populations. Arthritis Rheum. 64, 3687-3694 (2012).
9. Hiraki, L. T. et al. Ethnic differences in pediatric systemic lupus erythematosus. J. Rheumatol. 36, 2539-2546 (2009).
10. Mok, C. C., Tang, S. S., To, C. H. & Petri, M. Incidence and risk factors of thromboembolism in systemic lupus erythematosus: a comparison of three ethnic groups. Arthritis Rheum. 52, 2774-2782 (2005).
11. Costenbader, K. H. et al. Trends in the incidence, demographics, and outcomes of end-stage renal disease due to lupus nephritis in the US from 1995 to 2006. Arthritis Rheum. 63, 1681-1688 (2011).
12. Cottone, S. et al. Oxidative stress, inflammation and cardiovascular disease in chronic renal failure. J. Nephrol. 21, 175-179 (2008).
13. Mok, C. C. et al. Risk and predictors of arterial thrombosis in lupus and non-lupus primary glomerulonephritis: a comparative study. Med. (Baltimore) 86, 203-209 (2007).
14. Appenzeller, S. et al. The relationship between renal activity and quality of life in systemic lupus erythematosus. J. Rheumatol. 36, 947-952 (2009).
15. Mok, C. C., Cheung, M. Y., Ho, L. Y., Yu, K. L. & To, C. H. Risk and predictors of work disability in Chinese patients with systemic lupus erythematosus. Lupus 17, 1103-1107 (2008).
16. Felson, D. T. & Anderson, J. Evidence for the superiority of immunosuppressive drugs and prednisone over prednisone alone in lupus nephritis - results of a pooled analysis. N. Engl. J. Med. 311, 1528-1533 (1984).
17. Austin, H. A. 3rd et al. Therapy of lupus nephritis. N. Engl. J. Med. 314, 614-619 (1986).
18. Arends, S. et al. Long-term follow-up of a randomised controlled trial of azathioprine/methylprednisolone versus cyclophosphamide in patients with proliferative lupus nephritis. Ann. Rheum. Dis. 71, 966-973 (2012).
19. Houssiau, F. A. 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. 46, 2121-2131 (2002).
20. Houssiau, F. A. et al. The 10-year follow-up data of the Euro-Lupus Nephritis Trial comparing low-dose and high-dose intravenous cyclophosphamide. Ann. Rheum. Dis. 69, 61-64 (2010).
21. Mysler, E. F. et al. Efficacy and safety of ocrelizumab in active proliferative lupus nephritis: results from a randomized, double-blind, Phase III study. Arthritis Rheum. 65, 2368-2379 (2013).
22. ACCESS Trial Group. Treatment of lupus nephritis with abatacept: the Abatacept and Cyclophosphamide Combination Efficacy and Safety Study. Arthritis Rheumatol. 66, 3096-3104 (2014).
23. Hahn, B. H. et al. American College of Rheumatology guidelines for screening, treatment, and management of lupus nephritis. Arthritis Care Res. (Hoboken) 64, 797-808 (2012).
24. Bertsias, G. K. et al. Joint European League Against Rheumatism and European Renal Association-European Dialysis and Transplant Association (EULAR/ERA-EDTA) recommendations for the management of adult and paediatric lupus nephritis. Ann. Rheum. Dis. 71, 1771-1782 (2012).
25. Tang, Z. et al. Clinical features and renal outcome in lupus patients with diffuse crescentic glomerulonephritis. Rheumatol. Int. 30, 45-49 (2009).
26. Chan, T. M. et al. Efficacy of mycophenolate mofetil in patients with diffuse proliferative lupus nephritis. N. Engl. J. Med. 343, 1156-1162 (2000).
27. Ginzler, E. M. et al. Mycophenolate mofetil or intravenous cyclophosphamide for lupus nephritis. N. Engl. J. Med. 353, 2219-2228 (2005).
28. Appel, G. B. et al. Mycophenolate mofetil versus cyclophosphamide for induction treatment of lupus nephritis. J. Am. Soc. Nephrol. 20, 1103-1112 (2009).
29. Radhakrishnan, J. et al. Mycophenolate mofetil and intravenous cyclophosphamide are similar as induction therapy for class V lupus nephritis. Kidney Int. 77, 152-160 (2010).
30. Isenberg, D. et al. Influence of race/ethnicity on response to lupus nephritis treatment: the ALMS study. Rheumatol. (Oxford) 49, 128-140 (2010).
31. Mok, C. C. et al. Overview of lupus nephritis management guidelines and perspective from Asia. Nephrol. (Carlton) 19, 11-20 (2014).
32. Tang, Z. et al. Effects of mycophenolate mofetil for patients with crescentic lupus nephritis. Nephrol. (Carlton) 13, 702-707 (2008).
33. Rovin, B. H. et al. Lupus nephritis: induction therapy in severe lupus nephritis - should MMF be considered the drug of choice? Clin. J. Am. Soc. Nephrol. 8, 147-153 (2013).
34. Scott, L. J., McKeage, K., Keam, S. J. & Plosker, G. L. Tacrolimus: a further update of its use in the management of organ transplantation. Drugs 63, 1247-1297 (2003).
35. Ekberg, H. et al. Reduced exposure to calcineurin inhibitors in renal transplantation. N. Engl. J. Med. 357, 2562-2575 (2007).
36. Krämer, B. K. et al. Efficacy and safety of tacrolimus compared with ciclosporin A in renal transplantation: three-year observational results. Nephrol. Dial. Transplant. 23, 2386-2392 (2008).
37. Silva, H. T. Jr et al. Long-term follow-up of a Phase III clinical trial comparing tacrolimus extended-release/MMF, tacrolimus/MMF, and cyclosporine/MMF in de novo kidney transplant recipients. Transplantation 97, 636-641 (2014).
38. Penninga, L., Møller, C. H., Gustafsson, F., Steinbrüchel, D. A. & Gluud, C. Tacrolimus versus cyclosporine as primary immunosuppression after heart transplantation: systematic review with meta-analyses and trial sequential analyses of randomised trials. Eur. J. Clin. Pharmacol. 66, 1177-1187 (2010).
39. O'Keefe, S. J., Tamura, J., Kincaid, R. L., Tocci, M. J. & O'Neill, E. A. FK-506- and CsA-sensitive activation of the interleukin-2 promoter by calcineurin. Nature 357, 692-694 (1992).
40. Yoon, K. H. Efficacy and cytokine modulating effects of tacrolimus in systemic lupus erythematosus: a review. J. Biomed. Biotechnol. 2010, 686480 (2010).
41. Heidt, S. et al. Calcineurin inhibitors affect B cell antibody responses indirectly by interfering with T cell help. Clin. Exp. Immunol. 159, 199-207 (2010).
42. Faul, C. et al. The actin cytoskeleton of kidney podocytes is a direct target of the antiproteinuric effect of cyclosporine A. Nat. Med. 14, 931-938 (2008).
43. Mok, C. C., Tong, K. H., To, C. H., Siu, Y. P. & Au, T. C. Tacrolimus for induction therapy of diffuse proliferative lupus nephritis: an open-labeled pilot study. Kidney Int. 68, 813-817 (2005).
44. Szeto, C. C. et al. Tacrolimus for the treatment of systemic lupus erythematosus with pure class V nephritis. Rheumatol. (Oxford) 47, 1678-1681 (2008).
45. Chen, W. et al. Short-term outcomes of induction therapy with tacrolimus versus cyclophosphamide for active lupus nephritis: a multicenter randomized clinical trial. Am. J. Kidney Dis. 57, 235-244 (2011).
46. Li, X. et al. Mycophenolate mofetil or tacrolimus compared with intravenous cyclophosphamide in the induction treatment for active lupus nephritis. Nephrol. Dial. Transplant. 27, 1467-1472 (2012).
47. Mok, C. C. et al. Tacrolimus versus mycophenolate mofetil for induction therapy of lupus nephritis: a randomised controlled trial and long-term follow up. Ann. Rheum. Dis. http://dx.doi.org/10.1136/annrheumdis-2014-206456 (2014).
48. Bao, H. et al. Successful treatment of class V+IV lupus nephritis with multitarget therapy. J. Am. Soc. Nephrol. 19, 2001-2010 (2008).
49. Liu, Z. et al. Multitarget therapy for induction treatment of lupus nephritis: a randomized trial. Ann. Intern. Med. 162, 18-26 (2015).
50. Mok, C. C., To, C. H., Yu, K. L. & Ho, L. Y. Combined low-dose mycophenolate mofetil and tacrolimus for lupus nephritis with suboptimal response to standard therapy: a 12-month prospective study. Lupus 22, 1135-1141 (2013).
51. Mok, C. C. Membranous nephropathy in systemic lupus erythematosus: a therapeutic enigma. Nat. Rev. Nephrol. 5, 212-220 (2009).
52. Austin, H. A. 3rd, Illei, G. G., Braun, M. J. & Balow, J. E. Randomized, controlled trial of prednisone, cyclophosphamide, and cyclosporine in lupus membranous nephropathy. J. Am. Soc. Nephrol. 20, 901-911 (2009).
53. Jónsdóttir, T. et al. Clinical improvements in proliferative versus membranous lupus nephritis following B-cell depletion: pooled data from two cohorts. Rheumatol. (Oxford) 49, 1502-1504 (2010).
54. Illei, G. G. et al. Renal flares are common in patients with severe proliferative lupus nephritis treated with pulse immunosuppressive therapy: long-term follow up of a cohort of 145 patients participating in randomized controlled studies. Arthritis Rheum. 46, 995-1002 (2002).
55. Moroni, G. et al. A randomized pilot trial comparing cyclosporine and azathioprine for maintenance therapy in diffuse lupus nephritis over four years. Clin. J. Am. Soc. Nephrol. 1, 925-932 (2006).
56. Contreras, G. et al. Sequential therapies for proliferative lupus nephritis. N. Engl. J. Med. 350, 971-980 (2004).
57. Moroni, G. et al. Withdrawal of therapy in patients with proliferative lupus nephritis: long-term follow up. Nephrol. Dial. Transplant. 21, 1541-1548 (2006).
58. Chen, W. et al. Outcomes of maintenance therapy with tacrolimus versus azathioprine for active lupus nephritis: a multicenter randomized clinical trial. Lupus 21, 944-952 (2012).
59. Houssiau, F. A. et al. Azathioprine versus mycophenolate mofetil for long-term immunosuppression in lupus nephritis: results from the MAINTAIN Nephritis Trial. Ann. Rheum. Dis. 69, 2083-2089 (2010).
60. Tamirou, F. et al. Long-term follow-up of the MAINTAIN Nephritis Trial, comparing azathioprine and mycophenolate mofetil as maintenance therapy of lupus nephritis. Ann. Rheum. Dis. http://dx.doi.org/10.1136/annrheumdis-2014-206897 (2015).
61. Dooley, M. A. et al. Mycophenolate versus azathioprine as maintenance therapy for lupus nephritis. N. Engl. J. Med. 365, 1886-1895 (2011).
62. Mok, C. C. Prognostic factors for lupus nephritis. Lupus 14, 39-44 (2005).
63. Lenz, O., Waheed, A. A., Baig, A., Pop, A. & Contreras, G. Lupus nephritis: maintenance therapy for lupus nephritis - do we now have a plan? Clin. J. Am. Soc. Nephrol. 8, 162-171 (2013).
64. Mok, C. C. Emerging biological therapies for systemic lupus erythematosus. Expert Opin. Emerg. Drugs 19, 303-322 (2014).
65. Rovin, B. H. et al. Efficacy and safety of rituximab in patients with active proliferative lupus nephritis: the Lupus Nephritis Assessment with Rituximab study. Arthritis Rheum. 64, 1215-1226 (2012).
66. Fernández-Nebro, A. et al. Multicenter longitudinal study of B-lymphocyte depletion in refractory systemic lupus erythematosus: the LESIMAB study. Lupus 21, 1063-1076 (2012).
67. Ramos-Casals, M., Soto, M. J., Cuadrado, M. J. & Khamashta, M. A. Rituximab in systemic lupus erythematosus: a systematic review of off-label use in 188 cases. Lupus 18, 767-776 (2009).
68. Weidenbusch, M., Römmele, C., Schröttle, A. & Anders, H. J. Beyond the LUNAR trial. Efficacy of rituximab in refractory lupus nephritis. Nephrol. Dial. Transplant. 28, 106-111 (2013).
69. Díaz-Lagares, C. et al. Efficacy of rituximab in 164 patients with biopsy-proven lupus nephritis: pooled data from European cohorts. Autoimmun. Rev. 11, 357-364 (2012).
70. Terrier, B. et al. Safety and efficacy of rituximab in systemic lupus erythematosus: results from 136 patients from the French AutoImmunity and Rituximab registry. Arthritis Rheum. 62, 2458-2466 (2010).
71. Rovin, B. H. & Parikh, S. V. Lupus nephritis: the evolving role of novel therapeutics. Am. J. Kidney Dis. 63, 677-690 (2014).
72. Condon, M. B. et al. Prospective observational single centre cohort study to evaluate the effectiveness of treating lupus nephritis with rituximab and mycophenolate mofetil but no oral steroids. Ann. Rheum. Dis. 72, 1280-1286 (2013).
73. US National Library of Medicine. ClinicalTrials.gov [online], https://clinicaltrials.gov/ct2/show/NCT01773616 (2015).
74. Reddy, V., Jayne, D., Close, D. & Isenberg, D. B cell depletion in SLE: clinical and trial experience with rituximab and ocrelizumab and implications for study design. Arthritis Res. Ther. 15, S2 (2013).
75. Jacobi, A. M. et al. Effect of long-term belimumab treatment on B cells in systemic lupus erythematosus: extension of a Phase II, double-blind, placebo-controlled, dose-ranging study. Arthritis Rheum. 62, 201-210 (2010).
76. Navarra, S. V. et al. Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebo-controlled, Phase 3 trial. Lancet 377, 721-731 (2011).
77. Furie, R. et al. A Phase III, randomized, placebo-controlled study of belimumab, a monoclonal antibody that inhibits B lymphocyte stimulator, in patients with systemic lupus erythematosus. Arthritis Rheum. 63, 3918-3930 (2011).
78. Mok, C. C. Belimumab: the first FDA approved biological therapy for systemic lupus erythematosus. Int. J. Clin. Rheumatol. 6, 373-377 (2011).
79. Manzi, S. et al. Effects of belimumab, a B lymphocyte stimulator-specific inhibitor, on disease activity across multiple organ domains in patients with systemic lupus erythematosus: combined results from two Phase III trials. Ann. Rheum. Dis. 71, 1833-1838 (2012).
80. van Vollenhoven, R. F. et al. Belimumab in the treatment of systemic lupus erythematosus: high disease activity predictors of response. Ann. Rheum. Dis. 71, 1343-1349 (2012).
81. Dooley, M. A. et al. Effect of belimumab treatment on renal outcomes: results from the phase 3 belimumab clinical trials in patients with SLE. Lupus 22, 63-72 (2013).
82. US National Library of Medicine. ClinicalTrials.gov [online], https://clinicaltrials.gov/ct2/show/NCT01639339 (2015).
83. Stohl, W. Systemic lupus erythematosus and its ABCs (APRIL/BLyS complexes). Arthritis Res. Ther. 12, 111 (2010).
84. Ginzler, E. M. et al. Atacicept in combination with MMF and corticosteroids in lupus nephritis: results of a prematurely terminated trial. Arthritis Res. Ther. 14, R33 (2012).
85. Isenberg, D. et al. Efficacy and safety of atacicept for prevention of flares in patients with moderate-to-severe systemic lupus erythematosus (SLE): 52 week data (APRIL-SLE randomised trial). Ann. Rheum. Dis. 74, 2006-2015 (2015).
86. Mok, C. C. Abatacept for systemic lupus erythematosus: the outlook. Expert Opin. Biol. Ther. 12, 1559-1561 (2012).
87. Furie, R. et al. Efficacy and safety of abatacept in lupus nephritis: a twelve-month, randomized, double-blind study. Arthritis Rheumatol. 66, 379-389 (2014).
88. Daikh, D. I. & Wofsy, D. Cutting edge: reversal of murine lupus nephritis with CTLA4Ig and cyclophosphamide. J. Immunol. 166, 2913-2916 (2001).
89. Brück, W. & Zamvil, S. S. Laquinimod, a once-daily oral drug in development for the treatment of relapsing-remitting multiple sclerosis. Expert Rev. Clin. Pharmacol. 5, 245-256 (2012).
90. Jayne, D. et al. A randomized controlled study of laquinimod in active lupus nephritis patients in combination with standard of care. Ann. Rheum. Dis. 78, A164 (2013).
91. Michaelson, J. S., Wisniacki, N., Burkly, L. C. & Putterman, C. Role of TWEAK in lupus nephritis: a bench-to-bedside review. J. Autoimmun. 39, 130-142 (2012).
92. Schwartz, N. et al. Urinary TWEAK as a biomarker of lupus nephritis: a multicenter cohort study. Arthritis Res. Ther. 11, R143 (2009).
93. US National Library of Medicine. ClinicalTrials.gov [online], https://clinicaltrials.gov/ct2/show/NCT01499355 (2015).
94. Lertdumrongluk, P. et al. Pharmacokinetics of mycophenolic acid in severe lupus nephritis. Kidney Int. 78, 389-395 (2010).
95. Neumann, I. et al. Association between mycophenolic acid 12-h trough levels and clinical endpoints in patients with autoimmune disease on mycophenolate mofetil. Nephrol. Dial. Transplant. 23, 3514-3520 (2008).
96. Djabarouti, S. et al. Steady-state mycophenolate mofetil pharmacokinetic parameters enable prediction of systemic lupus erythematosus clinical flares: an observational cohort study. Arthritis Res. Ther. 12, R217 (2010).
97. Zahr, N. et al. Mycophenolic acid area under the curve correlates with disease activity in lupus patients treated with mycophenolate mofetil. Arthritis Rheum. 62, 2047-2054 (2010).
98. Mok, C. C. Biomarkers for lupus nephritis: a critical appraisal. J. Biomed. Biotechnol. 2010, 638413 (2010).
99. Li, Y., Fang, X. & Li, Q. Z. Biomarkers profiling for lupus nephritis. Genom. Proteom. Bioinformat. 11, 158-165 (2013).
100. Watson, L. & Beresford, M. W. Urine biomarkers in juvenile-onset SLE nephritis. Pediatr. Nephrol. 28, 363-374 (2013).
101. Hinze, C. H. et al. Neutrophil gelatinase-associated lipocalin is a predictor of the course of global and renal childhood-onset systemic lupus erythematosus disease activity. Arthritis Rheum. 60, 2772-2781 (2009).
102. Watson, L. et al. Urine biomarkers for monitoring juvenile lupus nephritis: a prospective longitudinal study. Pediatr. Nephrol. 29, 397-405 (2014).
103. Sui, W., Hou, X., Che, W., Yang, M. & Dai, Y. The applied basic research of systemic lupus erythematosus based on the biological omics. Genes Immun. 14, 133-146 (2013).
104. Verdecchia, P. et al. Usual versus tight control of systolic blood pressure in non-diabetic patients with hypertension (Cardio-Sis): an open-label randomised trial. Lancet 374, 525-533 (2009).
105. Fullerton, B. et al. Intensive glucose control versus conventional glucose control for type 1 diabetes mellitus. Cochrane Database Syst. Rev. 2, CD009122 (2014).
106. Stoffer, M. A. et al. Evidence for treating rheumatoid arthritis to target: results of a systematic literature search update. Ann. Rheum. Dis. http://dx.doi.org/10.1136/annrheumdis-2015-207526 (2015).
107. van Vollenhoven, R. F. et al. Treat-to-target in systemic lupus erythematosus: recommendations from an international task force. Ann. Rheum. Dis. 73, 958-967 (2014).
108. Mok, C. C. et al. Predictors and outcome of renal flares after successful cyclophosphamide treatment for diffuse proliferative lupus glomerulonephritis. Arthritis Rheum. 50, 2559-2568 (2004).
109. Moroni, G. et al. Membranous nephropathy in systemic lupus erythematosus: long-term outcome and prognostic factors of 103 patients. Semin. Arthritis Rheum. 41, 642-651 (2012).
110. Reich, H. N. et al. Persistent proteinuria and dyslipidemia increase the risk of progressive chronic kidney disease in lupus erythematosus. Kidney Int. 79, 914-920 (2011).
111. Griffin, B. & Lightstone, L. Renoprotective strategies in lupus nephritis: beyond immunosuppression. Lupus 22, 1267-1273 (2013).
112. Tang, C., Godfrey, T., Stawell, R. & Nikpour, M. Hydroxychloroquine in lupus: emerging evidence supporting multiple beneficial effects. Intern. Med. J. 42, 968-978 (2012).
113. Olsen, N. J., Schleich, M. A. & Karp, D. R. Multifaceted effects of hydroxychloroquine in human disease. Semin. Arthritis Rheum. 43, 264-272 (2013).
114. Pons-Estel, G. J. et al. Protective effect of hydroxychloroquine on renal damage in patients with lupus nephritis: LXV, data from a multiethnic US cohort. Arthritis Rheum. 61, 830-839 (2009).
115. Sisó, A. et al. Previous antimalarial therapy in patients diagnosed with lupus nephritis: influence on outcomes and survival. Lupus 17, 281-288 (2008).
116. Alarcón, G. S. et al. Effect of hydroxychloroquine on the survival of patients with systemic lupus erythematosus: data from LUMINA, a multiethnic US cohort (LUMINA L). Ann. Rheum. Dis. 66, 1168-1172 (2007).
117. Ruiz-Irastorza, G. et al. Effect of antimalarials on thrombosis and survival in patients with systemic lupus erythematosus. Lupus 15, 577-583 (2006).