Induction and maintenance treatment of proliferative lupus nephritis: A meta-analysis of randomized controlled trials

American Journal of Kidney Diseases

Volumn 61, Issue 1, 2013, Pages 74-87

  Henderson, Lorna K ^a,b   Masson, Philip ^a,c   Craig, Jonathan C ^a,c   Roberts, Matthew A ^d   Flanc, Robert S ^e   Strippoli, Giovanni F M ^a,c,f,g,h   Webster, Angela C ^a,b,c  

^a CHILDREN S HOSPITAL AT WESTMEAD   (Australia)

^b WESTMEAD HOSPITAL   (Australia)

^c UNIVERSITY OF SYDNEY   (Australia)

^d AUSTIN HEALTH   (Australia)

^e MONASH MEDICAL CENTRE   (Australia)

^f Mario Negri Sud Consortium ^*  (Italy)

^g Diaverum Medical Scientific Office   (Sweden)

^h UNIVERSITY OF BARI   (Italy)

Author keywords

cyclophosphamide (CYC); Lupus nephritis; meta analysis; mycophenolate mofetil (MMF); proliferative glomerulonephritis; systematic review; systemic lupus erythematosus (SLE)

Indexed keywords

AZATHIOPRINE; CORTICOSTEROID; CREATININE; CYCLOPHOSPHAMIDE; CYCLOSPORIN; CYCLOSPORIN A; HEPARIN; IMMUNOGLOBULIN; IMMUNOSUPPRESSIVE AGENT; METHYLPREDNISOLONE; MISOPROSTOL; MYCOPHENOLIC ACID; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; RITUXIMAB; STEROID; TACROLIMUS;

ALOPECIA; AVASCULAR NECROSIS; COCHRANE LIBRARY; CONFIDENCE INTERVAL; CREATININE BLOOD LEVEL; CREATININE CLEARANCE; DATA EXTRACTION; DIARRHEA; DISEASE CLASSIFICATION; DOSAGE SCHEDULE COMPARISON; DRUG DOSE REDUCTION; DRUG FATALITY; DRUG MEGADOSE; EMBASE; ENTERIC COATED TABLET; FRACTURE; GASTROINTESTINAL SYMPTOM; HERPES ZOSTER; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; INCIDENCE; KIDNEY FAILURE; LEUKOPENIA; LOW DRUG DOSE; LUPUS ERYTHEMATOSUS NEPHRITIS; MAINTENANCE THERAPY; MEDLINE; MEMBRANOUS GLOMERULONEPHRITIS; META ANALYSIS; MORTALITY; OUTCOME ASSESSMENT; OVARY INSUFFICIENCY; PHASE 1 CLINICAL TRIAL (TOPIC); PLASMAPHERESIS; PROLIFERATIVE GLOMERULONEPHRITIS; PROTEINURIA; RANDOMIZED CONTROLLED TRIAL (TOPIC); RELAPSE; REMISSION; REVIEW; RISK; SIDE EFFECT; SINGLE DRUG DOSE; SYSTEMATIC REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS; URINE SEDIMENT; VOMITING;

EID: 84871218981     PISSN: 02726386     EISSN: 15236838     Source Type: Journal    
DOI: 10.1053/j.ajkd.2012.08.041     Document Type: Article

References (83)

1. F.A. Houssiau, C. Vasconcelos, D. D'Cruz The 10-year follow-up data of the Euro-Lupus Nephritis Trial comparing low-dose and high-dose intravenous cyclophosphamide Ann Rheum Dis 69 1 2010 61 64
2. US Renal Data System USRDS 2011 Annual Data Report: Atlas of Chronic Kidney Disease and End-Stage Renal Disease in the United States Am J Kidney Dis 59 1 2012 e1 e420 (suppl 1)
3. B. Grace, L. Excell, H. Dent, S. Mc Donald New patients commencing treatment in 2009 S. Mc Donald, L. Excell, B. Livingston, ANZDATA Registry Report 2010 2010 Australia and New Zealand Dialysis and Transplant Registry Adelaide, South Australia 2.1 2.12
4. J.S. Cameron Lupus nephritis J Am Soc Nephrol 10 2 1999 413 424 (Pubitemid 29068083)
5. C.C. Mok, C.T. Ho, K.W. Chan, C.S. Lau, R.W. Wong Outcome and prognostic indicators of diffuse proliferative lupus glomerulonephritis treated with sequential oral cyclophosphamide and azathioprine Arthritis Rheum 46 4 2002 1003 1013 (Pubitemid 34303813)
6. C. Ponticelli, G. Moroni Flares in lupus nephritis: incidence, impact on renal survival and management Lupus 7 9 1998 635 638 (Pubitemid 29008231)
7. R.A. Hickman, C. Gordon Causes and management of infertility in systemic lupus erythematosus Rheumatology 50 9 2011 1551 1558
8. R.S. Flanc, M.A. Roberts, G.F. Strippoli, S.J. Chadban, P.G. Kerr, R.C. Atkins Treatment of diffuse proliferative lupus nephritis: a meta-analysis of randomized controlled trials Am J Kidney Dis 43 2 2004 197 208
9. R.S. Flanc, M.A. Roberts, G.F. Strippoli, S.J. Chadban, P.G. Kerr, R.C. Atkins Treatment for lupus nephritis Cochrane Database Syst Rev 1 2004 CD002922
10. C. Grootscholten, G. Ligtenberg, E.C. Hagen Azathioprine/ methylprednisolone versus cyclophosphamide in proliferative lupus nephritis A randomized controlled trial Kidney Int 70 4 2006 732 742 (Pubitemid 44215349)
11. D.R. Jayne, M. Zeher Enteric-coated mycophenolate sodium (ED-MPS) for the treatment of lupus nephritis-My Lupus Study [abstract] J Am Soc Nephrol 21 2010 626A
12. Sundel RP, Lisk L. Mycophenolate mofetil compared with intravenous cyclophosphamide as induction treatment for pediatric lupus nephritis: a randomized trial. Paper presented at: American College of Rheumatology Annual Scientific Meeting; October 24-29, 2008; San Francisco, CA.
13. C.C. Mok, S.K. Ying, K.H. Tong Mycophenolate mofetil versus tacrolimus for active lupus nephritis: an extended observation of a randomized controlled trial Ann Rheum Dis 68 suppl 3 2009 246
14. F.A. Houssiau, D. D'Cruz, S. Sangle Azathioprine versus mycophenolate mofetil for long-term immunosuppression in lupus nephritis: results from the MAINTAIN Nephritis Trial Ann Rheum Dis 69 12 2010 2083 2089
15. X. Li, H. Ren, W. Zhang, Y. Xu, P. Shen, Q. Zhang Induction therapies for proliferative lupus nephritis: mycophenolate mofetil, tacrolimus and intravenous cyclophosphamide [abstract] J Am Soc Nephrol 20 2009 391A
16. G.B. Appel, G. Contreras, M.A. Dooley Mycophenolate mofetil versus cyclophosphamide for induction treatment of lupus nephritis J Am Soc Nephrol 20 5 2009 1103 1112
17. H. Bao, Z.H. Liu, H.L. Xie, W.X. Hu, H.T. Zhang, L.S. Li Successful treatment of class V+IV lupus nephritis with multitarget therapy J Am Soc Nephrol 19 10 2008 2001 2010
18. G. Contreras, E. Tozman, N. Nahar, D. Metz Maintenance therapies for proliferative lupus nephritis: mycophenolate mofetil, azathioprine and intravenous cyclophosphamide Lupus 14 suppl 1 2005 s33 s38
19. E.M. Ginzler, M.A. Dooley, C. Aranow Mycophenolate mofetil or intravenous cyclophosphamide for lupus nephritis N Engl J Med 353 21 2005 2219 2228 (Pubitemid 41697285)
20. E.K. Li, L.S. Tam, T.Y. Zhu Is combination rituximab with cyclophosphamide better than rituximab alone in the treatment of lupus nephritis? Rheumatology 48 8 2009 892 898
21. Furie R, Looney RJ, Rovin B, Latinis KM, et al. Efficacy and safety of rituximab in subjects with active proliferative lupus nephritis (LN): results from the randomized, double-blind phase III LUNAR study. Paper presented at: American College of Rheumatology Annual Scientific Meeting; October 17-21, 2009; Philadelphia, PA.
22. M. Zeher, J. Lan, A. Doria, Z. Amoura, D. Jayne, F. Hiepe Enteric coated mycophenolate sodium (EC-MPS) treatment of lupus nephritis flare-interim results from a multicentre, randomized trial Ann Rheum Dis 68 suppl 3 2009 250
23. J.P.T. Higgins, S. Green Cochrane Handbook for Systematic Reviews of Interventions Version 5.0.2 [updated September 2009] 2009 The Cochrane Collaboration www.cochrane-handbook.org Accessed November 13, 2012
24. J.P. Higgins, S.G. Thompson, J.J. Deeks, D.G. Altman Measuring inconsistency in meta-analyses BMJ 327 7414 2003 557 560 (Pubitemid 37088507)
25. J.J. Deeks Systematic reviews in health care: systematic reviews of evaluations of diagnostic and screening tests BMJ 323 7305 2001 157 162 (Pubitemid 32678396)
26. T.M. Chan, F.K. Li, C.S. Tang Efficacy of mycophenolate mofetil in patients with diffuse proliferative lupus nephritis Hong Kong-Guangzhou Nephrology Study Group N Engl J Med 343 16 2000 1156 1162
27. L.M. Ong, L.S. Hooi, T.O. Lim Randomized controlled trial of pulse intravenous cyclophosphamide versus mycophenolate mofetil in the induction therapy of proliferative lupus nephritis Nephrology 10 5 2005 504 510 (Pubitemid 41727277)
28. S. Mulic-Bacic, D. Antic, M. Krizic, A. Hajdarovic, E. Mulic Mycophenolate mofetil or intravenous cyclophosphamide in treatment of lupus nephritis Ann Rheum Dis 67 Suppl II 2008 349
29. E.M. El-Shafey, S.H. Abdou, M.M. Shareef Is mofetil superior to pulse intravenous cyclophosphamide for induction therapy of proliferative lupus nephritis in Egyptian patients? Clin Exp Nephrol 14 3 2010 214 221
30. A.D. Steinberg, H.B. Kaltreider, P.J. Staples, E.J. Goetzl, N. Talal, J.L. Decker Cyclophosphamide in lupus nephritis: a controlled trial Ann Intern Med 75 2 1971 165 171
31. J.F. Fries, G.C. Sharp, H.O. McDevitt, H.R. Holman Cyclophosphamide therapy in systemic lupus erythematosus and polymyositis Arthritis Rheum 16 2 1973 154 162
32. E. Ginzler, H. Diamond, M. Guttadauria, D. Kaplan Prednisone and azathioprine compared to prednisone plus low-dose azathioprine and cyclophosphamide in the treatment of diffuse lupus nephritis Arthritis Rheum 19 4 1976 693 699
33. J.V. Donadio Jr, K.E. Holley, R.H. Ferguson, D.M. Ilstrup Treatment of diffuse proliferative lupus nephritis with prednisone and combined prednisone and cyclophosphamide N Engl J Med 299 21 1978 1151 1155 (Pubitemid 9065570)
34. H.A. Austin III, J.H. Klippel, J.E. Balow Therapy of lupus nephritis Controlled trial of prednisone and cytotoxic drugs N Engl J Med 314 10 1986 614 619 (Pubitemid 16132725)
35. R. Sesso, M. Monteiro, L. Silva, E. Sato, H. Ajzen Pulse cyclophosphamide (cy) versus pulse methylprednisolone (mp) in severe lupus nephriitis [abstract] J Am Soc Nephrol 4 1993 286 Program & Abstracts
36. M.F. Gourley, H.A. Austin III, D. Scott Methylprednisolone and cyclophosphamide, alone or in combination, in patients with lupus nephritis A randomized, controlled trial Ann Intern Med 125 7 1996 549 557 (Pubitemid 126450087)
37. S.F. Lui, I.K.P. Cheng, K.L. Tong et al. Treatment of type IV lupus nephritis (LN)-comparison of 2 triple therapy regimens: cyclosporin a (CSA), prednisolone (PRED), azathioprine (AZA) vs. oral cyclophosphamide (POCP), prednisolone, azathioprine [abstract] Nephrology 3 Suppl 1 1997 S476
38. A.G. Adam, M.S. El Sehemy, N.M. Baddour, P.E. Moez, A.M. Al Saaran Prospective comparative study between azathiporpine "AZA", cyclophosphamide "CYP", cyclosporine "CsA" and mycophenolate mofitle "MMF" in the treatment of lupus nephritis: is CYP still the preferred therapy against the new-comer MMF? AZA: an old drug with still a great potential? [abstract F-P0258] J Am Soc Nephrol 15 2004 122A
39. O.I. Dyadyk, I. Vasilenko, A.E. Bagriy et al. Azathioprine and cyclophosphamide in diffuse proliferative lupus nephritis treatment-a randomized controlled study [abstract SAT0125] Ann Rheum Dis 66 Suppl II 2007 467
40. R. Hong, Y. Haijin, W. Xianglin, H. Cuilan, C. Nan A preliminary study of tacrolimus versus cyclophosphamide in patients with diffuse proliferative lupus nephritis [abstract SAP131] Nephrol Dial Transplantation 22 Suppl 6 2007 vi276
41. W. Chen, X. Tang, Q. Liu Short-term outcomes of induction therapy with tacrolimus versus cyclophosphamide for active lupus nephritis: a multicenter randomized clinical trial Am J Kidney Dis 57 2 2011 235 244
42. F.A. Houssiau, C. Vasconcelos, D. D'Cruz Immunosuppressive therapy in lupus nephritis: the Euro-Lupus Nephritis Trial, a randomized trial of low-dose versus high-dose intravenous cyclophosphamide Arthritis Rheum 46 8 2002 2121 2131
43. A. Sabry, H. Abo-Zenah, T. Medhat, H. Sheashaa, K. Mahmoud, A. El Huseini A comparative study of two intensified pulse cyclophosphamide remission-inducing regimens for diffuse proliferative lupus nephritis: an Egyptian experience Int Urol Nephrol 41 1 2009 153 161
44. A.H. Mitwalli, J.S. Al Wakeel, S. Hurraib et al. Comparison of high and low dose of cyclophosphamide in lupus nephritis patients: a long-term randomized controlled trial Saudi J Kidney Dis Transpl 22 5 2011 935 940
45. C.S. Yee, C. Gordon, C. Dostal EULAR randomised controlled trial of pulse cyclophosphamide and methylprednisolone versus continuous cyclophosphamide and prednisolone followed by azathioprine and prednisolone in lupus nephritis Ann Rheum Dis 63 5 2004 525 529 (Pubitemid 38530195)
46. D.T. Boumpas, H.A. Austin III, E.M. Vaughn Controlled trial of pulse methylprednisolone versus two regimens of pulse cyclophosphamide in severe lupus nephritis Lancet 340 8822 1992 741 745
47. B. Hahn, O. Kantor, C. Osterland Azathioprine plus prednisone compared with prednisone alone in the treatment of systemic lupus erythematosus Report of a prospective controlled trial in 24 patients Ann Intern Med 83 5 1975 597 605
48. M. Balletta, D. Sabella, P. Magri Ciclosporin plus corticosteroids versus corticosteroids alone in the treatment of lupus nephritis Contrib Nephrol 99 1992 129 130
49. H.M. Belmont, E. Kitsis, M.L. Skovron, J. Buyon, E. McCullagh, S. Abramson Misoprostol and prednisone treatment of lupus nephritis Am J Ther 2 12 1995 928 932
50. R. Cade, G. Spooner, E. Schlein et al. Comparison of azathioprine, prednisone, and heparin alone or combined in treating lupus nephritis Nephron 10 1 1973 37 56
51. K.S. Barron, D.A. Person, E.J. Brewer Jr, M.G. Beale, A.M. Robson Pulse methylprednisolone therapy in diffuse proliferative lupus nephritis J Pediatr 101 1 1982 137 141 (Pubitemid 12078193)
52. W.F. Clark, R.M. Lindsay, D.C. Cattran, W.B. Chodirker, C.C. Barnes, A.L. Linton Monthly plasmapheresis for systemic lupus erythematosus with diffuse proliferative glomerulonephritis: a pilot study Can Med Assoc J 125 2 1981 171 174 (Pubitemid 11047401)
53. W.F. Clark, J.W. Balfe, D.C. Cattran, W. Williams, R.M. Lindsay, A.L. Linton Long-term plasma exchange in patients with systemic lupus erythematosus and diffuse proliferative glomerulonephritis Plasma Ther Transfusion Technol 5 3 1984 353 360 (Pubitemid 14000064)
54. A. Doria, A. Piccoli, P. Vesco et al. Therapy of lupus nephritis A two-year prospective study Ann Med Interne (Paris) 145 5 1994 307 311 (Pubitemid 24349874)
55. E.J. Lewis, L.G. Hunsicker, S.P. Lan, R.D. Rohde, J.M. Lachin A controlled trial of plasmapheresis therapy in severe lupus nephritis The Lupus Nephritis Collaborative Study Group N Engl J Med 326 21 1992 1373 1379
56. D.J. Wallace, D. Goldfinger, S.H. Pepkowitz et al. Randomized controlled trial of pulse/synchronization cyclophosphamide/apheresis for proliferative lupus nephritis J Clin Apher 13 4 1998 163 166 (Pubitemid 29029275)
57. R.H. Derksen, R.J. Hene, C.G. Kallenberg, R.N. Valentijn, L. Kater Prospective multi-centre trial on the short-term effects of plasma exchange versus cytotoxic drugs in corticosteroid-resistant lupus nephritis Neth J Med 33 3-4 1988 168 177
58. T. Nakamura, C. Ushiyama, M. Hara et al. Comparative effects of plasmapheresis and intravenous cyclophosphamide on urinary podocyte excretion in patients with proliferative Lupus nephritis Clin Nephrol 57 2 2002 108 113 (Pubitemid 34145193)
59. D.R. Jayne, G.B. Appel, M.A. Dooley Results of the Aspreva Lupus Management Study (ALMS) maintenance phase [abstract] J Am Soc Nephrol 21 2010 25A
60. L.W. Fu, L.Y. Yang, W.P. Chen, C.Y. Lin Clinical efficacy of cyclosporin A Neoral in the treatment of paediatric lupus nephritis with heavy proteinuria Br J Rheumatol 37 2 1998 217 221
61. J.N. Boletis, J.P. Ioannidis, K.A. Boki, H.M. Moutsopoulos Intravenous immunoglobulin compared with cyclophosphamide for proliferative lupus nephritis Lancet 354 9178 1999 569 570 (Pubitemid 29381378)
62. J.N. Boletis, C. Boki, S. Michael, D.N. Stamatiadis, L. Nakopoulou, C. Moutsopoulos Comparative study of pulse treatment with cyclophosphamide or immunoglobulin to sustain the remission of lupus nephritis [abstract] J Am Soc Nephrol 9 1998 140A 141A
63. J. Zavada, S. Pesickova, R. Rysava Cyclosporine A or intravenous cyclophosphamide for lupus nephritis: the Cylofa-Lune Study Lupus 19 11 2010 1281 1289
64. G. Moroni, A. Doria, M. Mosca A randomized pilot trial comparing cyclosporine and azathioprine for maintenance therapy in diffuse lupus nephritis over four years Clin J Am Soc Nephrol 1 5 2006 925 932
65. G. Moroni, A. Doria, M. Mosca A randomized trial comparing cyclosporine versus azathioprine for maintenance therapy in diffuse lupus nephritis [abstract] J Am Soc Nephrol 15 2004 121A
66. J.V. Donadio Jr, K.E. Holley, R.D. Wagoner, R.H. Ferguson, F.C. McDuffie Further observations on the treatment of lupus nephritis with prednisone and combined prednisone and azathioprine Arthritis Rheum 17 5 1974 573 581
67. E.J. Lewis Plasmapheresis therapy is ineffective in SLE Lupus Nephritis Collaborative Study Group J Clin Apher 7 3 1992 153 (Pubitemid 23046793)
68. A. Mak, A.A.C. Cheak, J.Y.S. Tan, H.C. Su, R.C.M. Ho, C.S. Lau Mycophenolate mofetil is as efficacious as, but safer than, cyclophosphamide in the treatment of proliferative lupus nephritis: a meta-analysis and meta-regression Rheumatology 48 8 2009 944 952
69. R.A. Moore, S. Derry Systematic review and meta-analysis of randomised trials and cohort studies of mycophenolate mofetil in lupus nephritis Arthritis Res Ther 8 6 2006 1 10
70. N. Kamanamool, M. McEvoy, J. Attia Efficacy and adverse events of mycophenolate mofetil versus cyclophosphamide for induction therapy of lupus nephritis: systematic review and meta-analysis Medicine 89 4 2010 227 235
71. J. Radhakrishnan, D.A. Moutzouris, E.M. Ginzler, N. Solomons, I.I. Siempos, G.B. Appel Mycophenolate mofetil and intravenous cyclophosphamide are similar as induction therapy for class V lupus nephritis Kidney Int 77 2 2009 152 160
72. Z. Touma, D.D. Gladman, M.B. Urowitz, J. Beyene, E.M. Uleryk, P.S. Shah Mycophenolate mofetil for induction treatment of lupus nephritis: a systematic review and meta-analysis J Rheumatol 38 1 2011 69 78
73. M. Walsh, M. James, D. Jayne, M. Tonelli, B.J. Manns, B.R. Hemmelgam Mycophenolate mofetil for induction therapy of lupus nephritis: a systematic review and meta-analysis Clin J Am Soc Nephrol 2 5 2007 968 975
74. B. Zhu, N. Chen, Y. Lin, H. Ren, W. Zhang, W. Wang Mycophenolate mofetil in induction and maintenance therapy of severe lupus nephritis: a meta-analysis of randomized controlled trials Nephrol Dial Transplant 22 7 2007 1933 1942 (Pubitemid 47244763)
75. Y. Lee, J.H. Woo, S.J. Choi, J.D. Ji, G.G. Song Induction and maintenance therapy for lupus nephritis: a systematic review and meta-analysis Lupus 19 6 2010 703 710
76. A.C. Tricco, J. Tetzlaff, M. Sampson, D. Fergusson, E. Cogo, T. Horsley, D. Moher Few systematic reviews exist documenting the extent of bias: a systematic review J Clin Epidemiol 61 5 2008 422 434 (Pubitemid 351446187)
77. J.P. Ioannidis, K.A. Boki, M.E. Katsorida Remission, relapse, and re-remission of proliferative lupus nephritis treated with cyclophosphamide Kidney Int 57 1 2000 258 264 (Pubitemid 30227773)
78. S.M. Korbet, M.M. Schwartz, J. Evans, E.J. Lewis Collaborative Study Group Severe lupus nephritis: racial differences in presentation and outcome J Am Soc Nephrol 18 1 2007 244 254 (Pubitemid 46070148)
79. M.A. Dooley, S. Hogan, C. Jennette, R. Falk Cyclophosphamide therapy for lupus nephritis: poor renal survival in black Americans Glomerular Disease Collaborative Network Kidney Int 51 4 1997 1188 1195 (Pubitemid 27186545)
80. M. Adler, S. Chambers, C. Edwards, G. Neild, D. Isenberg An assessment of renal failure in an SLE cohort with special reference to ethnicity, over a 25-year period Rheumatology 45 9 2006 1144 1147 (Pubitemid 44542106)
81. G. Contreras, O. Lenz, V. Pardo Outcomes in African Americans and Hispanics with lupus nephritis Kidney Int 69 10 2006 1846 1851 (Pubitemid 43739214)
82. D. Moher, D.J. Cook, S. Eastwood, I. Olkin, D. Rennie, D.F. Stroup Improving the quality of reports of meta-analyses of randomised controlled trials: the QUOROM statement. Quality of Reporting of Meta-analyses Lancet 354 9193 1999 1896 1900
83. C. Begg, M. Cho, S. Eastwood, R. Horton, D. Moher, I. Olkin Improving the quality of reporting of randomized controlled trials The CONSORT statement JAMA 276 8 1996 637 639 (Pubitemid 26278070)