Table of Contents Author Guidelines Submit a Manuscript
International Journal of Rheumatology
Volume 2013 (2013), Article ID 347520, 9 pages
http://dx.doi.org/10.1155/2013/347520
Review Article

Adverse Event Burden, Resource Use, and Costs Associated with Immunosuppressant Medications for the Treatment of Systemic Lupus Erythematosus: A Systematic Literature Review

1GlaxoSmithKline, U.S. Health Outcomes, 5 Moore Drive, Research Triangle Park, NC 27709, USA
2United BioSource Corporation, 7101 Wisconsin Avenue Suite 600, Bethesda, MD 20814, USA
3Human Genome Sciences, Medical Affairs, 14200 Shady Grove Road, Rockville, MD 20850, USA
4Washington Hospital Center, Division of Rheumatology, 110 Irving Street NW, Washington, DC 20010, USA

Received 14 December 2012; Revised 17 February 2013; Accepted 25 February 2013

Academic Editor: Kenneth C. Kalunian

Copyright © 2013 A. Oglesby et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. G. Childs, “The pathogenesis of systemic lupus erythematosus,” Orthopaedic Nursing, vol. 25, no. 2, pp. 140–145, 2006. View at Google Scholar
  2. G. S. Cooper, M. A. Dooley, E. L. Treadwell, E. W. St Clair, C. G. Parks, and G. S. Gilkeson, “Hormonal, environmental, and infectious risk factors for developing systemic lupus erythematosus,” Arthritis & Rheumatism, vol. 41, no. 10, pp. 1714–1724, 1998. View at Google Scholar
  3. P. Panopalis and A. E. Clarke, “Systemic lupus erythematosus: clinical manifestations, treatment and economics,” Expert Review of Pharmacoeconomics and Outcomes Research, vol. 6, no. 5, pp. 563–575, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. D. P. D'Cruz, M. A. Khamashta, and G. R. Hughes, “Systemic lupus erythematosus,” The Lancet, vol. 369, no. 9561, pp. 587–596, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. K. Kalunian and T. M. Joan, “New directions in the treatment of systemic lupus erythematosus,” Current Medical Research & Opinion, vol. 25, no. 6, pp. 1501–1514, 2009. View at Google Scholar
  6. C. Yildirim-Toruner and B. Diamond, “Current and novel therapeutics in the treatment of systemic lupus erythematosus,” Journal of Allergy and Clinical Immunology, vol. 127, no. 2, pp. 303–312, 2011. View at Google Scholar
  7. R. Furie, W. Stohl, E. M. Ginzler et al., “Biologic activity and safety of belimumab, a neutralizing anti-B-lymphocyte stimulator (BLyS) monoclonal antibody: a phase I trial in patients with systemic lupus erythematosus,” Arthritis Research and Therapy, vol. 10, no. 5, article R109, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. “Guidelines for referral and management of systemic lupus erythematosus in adults. American College of Rheumatology Ad Hoc Committee on Systemic Lupus Erythematosus Guidelines,” Arthritis & Rheumatism, vol. 42, no. 9, pp. 1785–1796, 1999.
  9. R. A. Moore and S. Derry, “Systematic review and meta-analysis of randomised trials and cohort studies of mycophenolate mofetil in lupus nephritis,” Arthritis Research and Therapy, vol. 8, article R182, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. N. Kamanamool, M. McEvoy, J. Attia, A. Ingsathit, P. Ngamjanyaporn, and A. Thakkinstian, “Efficacy and adverse events of mycophenolate mofetil versus cyclophosphamide for induction therapy of lupus nephritis: systematic review and meta-analysis,” Medicine, vol. 89, no. 4, pp. 227–235, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. Y. H. Lee, J. H. Woo, S. J. Choi, J. D. Ji, and G. G. Song, “Induction and maintenance therapy for lupus nephritis: a systematic review and meta-analysis,” Lupus, vol. 19, no. 6, pp. 703–710, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. Z. Touma, D. D. Gladman, M. B. Urowitz, J. Beyene, E. M. Uleryk, and P. S. Shah, “Mycophenolate mofetil for induction treatment of lupus nephritis: a systematic review and metaanalysis,” Journal of Rheumatology, vol. 38, no. 1, pp. 69–78, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. G. Schmajuk and J. Yazdany, “Drug monitoring in systemic lupus erythematosus: a systematic review,” Seminars in Arthritis and Rheumatism, vol. 40, no. 6, pp. 559–575, 2011. View at Google Scholar
  14. J. T. Swan, D. M. Riche, K. D. Riche, and V. Majithia, “Systematic review and meta-analysis of immunosuppressant therapy clinical trials in membranous lupus nephritis,” Journal of Investigative Medicine, vol. 59, no. 2, pp. 246–258, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. Z. Touma, M. Urowitz, and D. Gladman, “Systematic review and meta-analysis of randomized trials for mycophenolic acid and mycophenolate mofetil for induction treatment of lupus nephritis,” Journal of Rheumatology, vol. 37, no. 6, pp. 1310–1311, 2010. View at Google Scholar · View at Scopus
  16. E. Sarnes, L. Crofford, M. Watson, G. Dennis, H. Kan, and D. Bass, “Incidence and US costs of corticosteroid-associated adverse events: a systematic literature review,” Clinical Therapeutics, vol. 33, no. 10, pp. 1413–1432, 2011. View at Google Scholar
  17. G. B. Appel, G. Contreras, M. A. Dooley et al., “Mycophenolate mofetil versus cyclophosphamide for induction treatment of lupus nephritis,” Journal of the American Society of Nephrology, vol. 20, no. 5, pp. 1103–1112, 2009. View at Google Scholar
  18. T. M. Chan, K. C. Tse, C. S. Tang, M. Y. Mok, and F. K. Li, “Hong Kong Nephrology Study Group. Long-term study of mycophenolate mofetil as continuous induction and maintenance treatment for diffuse proliferative lupus nephritis,” Journal of the American Society of Nephrology, vol. 16, no. 4, pp. 1076–1084, 2005. View at Google Scholar
  19. G. Contreras, V. Pardo, B. Leclercq et al., “Sequential therapies for proliferative lupus nephritis,” The New England Journal of Medicine, vol. 350, no. 10, pp. 971–980, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. G. Contreras, E. Tozman, N. Nahar, and D. Metz, “Maintenance therapies for proliferative lupus nephritis: mycophenolate mofetil, azathioprine and intravenous cyclophosphamide,” Lupus, vol. 14, no. 3, supplement 1, pp. S33–S38, 2005. View at Google Scholar · View at Scopus
  21. J. Cortés-Hernández, M. T. Torres-Salido, A. S. Medrano, M. V. Tarrés, and J. Ordi-Ros, “Long-term outcomes—mycophenolate mofetil treatment for lupus nephritis with addition of tacrolimus for resistant cases,” Nephrology Dialysis Transplantation, vol. 25, no. 12, pp. 3939–3948, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. E. M. Ginzler, M. A. Dooley, C. Aranow et al., “Mycophenolate mofetil or intravenous cyclophosphamide for lupus nephritis,” The New England Journal of Medicine, vol. 353, no. 21, pp. 2219–2228, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. F. A. Houssiau, C. Vasconcelos, D. D'Cruz et al., “The 10-year follow-up data of the Euro-Lupus Nephritis Trial comparing low-dose and high-dose intravenous cyclophosphamide,” Annals of the Rheumatic Diseases, vol. 69, no. 1, pp. 61–64, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. D. Isenberg, G. B. Appel, G. Contreras et al., “Influence of race/ethnicity on response to lupus nephritis treatment: the ALMS study,” Rheumatology, vol. 49, no. 1, pp. 128–140, 2010. View at Google Scholar · View at Scopus
  25. F. Lu, Y. Tu, X. Peng et al., “A prospective multicentre study of mycophenolate mofetil combined with prednisolone as induction therapy in 213 patients with active lupus nephritis,” Lupus, vol. 17, no. 7, pp. 622–629, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. C. N. Pisoni, F. J. Sanchez, Y. Karim et al., “Mycophenolate mofetil in systemic lupus erythematosus: efficacy and tolerability in 86 patients,” Journal of Rheumatology, vol. 32, no. 6, pp. 1047–1052, 2005. View at Google Scholar · View at Scopus
  27. M. M. Riskalla, E. C. Somers, R. A. Fatica, and W. J. McCune, “Tolerability of mycophenolate mofetil in patients with systemic lupus erythematosus,” Journal of Rheumatology, vol. 30, no. 7, pp. 1508–1512, 2003. View at Google Scholar · View at Scopus
  28. Z. Tang, G. Yang, C. Yu et al., “Effects of mycophenolate mofetil for patients with crescentic lupus nephritis,” Nephrology, vol. 13, no. 8, pp. 702–707, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. P. R. Fortin, M. Abrahamowicz, D. Ferland, D. Lacaille, C. D. Smith, and M. Zummer, “Steroid-sparing effects of methotrexate in systemic lupus erythematosus: a double-blind, randomized, placebo-controlled trial,” Arthritis Care and Research, vol. 59, no. 12, pp. 1796–1804, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. E. M. McDermott and R. J. Powell, “Incidence of ovarian failure in systemic lupus erythematosus after treatment with pulse cyclophosphamide,” Annals of the Rheumatic Diseases, vol. 55, no. 4, pp. 224–229, 1996. View at Google Scholar · View at Scopus
  31. H. A. Austin, J. H. Klippel, J. E. Balow et al., “Therapy of lupus nephritis. Controlled trial of prednisone and cytotoxic drugs,” The New England Journal of Medicine, vol. 314, no. 10, pp. 614–619, 1986. View at Google Scholar
  32. S. Carette, J. H. Klippel, J. L. Decker et al., “Controlled studies of oral immunosuppressive drugs in lupus nephritis. A long-term follow-up,” Annals of Internal Medicine, vol. 99, no. 1, pp. 1–8, 1983. View at Google Scholar
  33. B. Griffiths, P. Emery, V. Ryan et al., “The BILAG multi-centre open randomized controlled trial comparing ciclosporin vs azathioprine in patients with severe SLE,” Rheumatology, vol. 49, no. 4, pp. 723–732, 2010. View at Google Scholar · View at Scopus
  34. G. Moroni, A. Doria, M. Mosca et al., “A randomized pilot trial comparing cyclosporine and azathioprine for maintenance therapy in diffuse lupus nephritis over four years,” Clinical Journal of the American Society of Nephrology, vol. 1, no. 5, pp. 925–932, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. M. A. Naughton, E. Battaglia, S. O'Brien, M. J. Walport, and M. Botto, “Identification of thiopurine methyltransferase (TPMT) polymorphisms cannot predict myelosuppression in systemic lupus erythematosus patients taking azathioprine,” Rheumatology, vol. 38, no. 7, pp. 640–644, 1999. View at Publisher · View at Google Scholar · View at Scopus
  36. C. C. Mok, C. S. Lau, and R. W. S. Wong, “Risk factors for ovarian failure in patients with systemic lupus erythematosus receiving cyclophosphamide therapy,” Arthritis & Rheumatism, vol. 41, no. 5, pp. 831–837, 1998. View at Google Scholar
  37. W. Chen, X. Tang, Q. Liu et al., “Short-term outcomes of induction therapy with tacrolimus versus cyclophosphamide for active lupus nephritis: a multicenter randomized clinical trial,” American Journal of Kidney Diseases, vol. 57, no. 2, pp. 235–244, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. M. F. Gourley, H. A. Austin, D. Scott et al., “Methylprednisolone and cyclophosphamide, alone or in combination, in patients with lupus nephritis: a randomized, controlled trial,” Annals of Internal Medicine, vol. 125, no. 7, pp. 549–557, 1996. View at Google Scholar · View at Scopus
  39. F. A. Houssiau, C. Vasconcelos, D. D'Cruz et al., “Immunosuppressive therapy in lupus nephritis: the Euro-Lupus Nephritis Trial, a randomized trial of low-dose versus high-dose intravenous cyclophosphamide,” Arthritis and Rheumatism, vol. 46, no. 8, pp. 2121–2131, 2002. View at Publisher · View at Google Scholar · View at Scopus
  40. G. G. Illei, H. A. Austin, M. Crane et al., “Combination therapy with pulse cyclophosphamide plus pulse methylprednisolone improves long-term renal outcome without adding toxicity in patients with lupus nephritis,” Annals of Internal Medicine, vol. 135, no. 4, pp. 248–257, 2001. View at Google Scholar
  41. J. P. A. Ioannidis, G. E. Katsifis, A. G. Tzioufas, and H. M. Moutsopoulos, “Predictors of sustained amenorrhea from pulsed intravenous cyclophosphamide in premenopausal women with systemic lupus erythematosus,” Journal of Rheumatology, vol. 29, no. 10, pp. 2129–2135, 2002. View at Google Scholar · View at Scopus
  42. L. Liang, X. Yang, H. Xu et al., “Clinical predictors of recovery and complications in the management of recent-onset renal failure in lupus nephritis: a Chinese experience,” Journal of Rheumatology, vol. 31, no. 4, pp. 701–706, 2004. View at Google Scholar · View at Scopus
  43. K. Manger, L. Wildt, J. R. Kalden, and B. Manger, “Prevention of gonadal toxicity and preservation of gonadal function and fertility in young women with systemic lupus erythematosus treated by cyclophosphamide: the PREGO-Study,” Autoimmunity Reviews, vol. 5, no. 4, pp. 269–272, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. C. C. Mok, K. Y. Ying, W. L. Ng et al., “Long-term outcome of diffuse proliferative lupus glomerulonephritis treated with cyclophosphamide,” American Journal of Medicine, vol. 119, no. 4, pp. 355.e25–355.e33, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. B. D. Pryor, S. G. Bologna, and L. E. Kahl, “Risk factors for serious infection during treatment with cyclophosphamide and high-dose corticosteroids for systemic lupus erythematosus,” Arthritis and Rheumatism, vol. 39, no. 9, pp. 1475–1482, 1996. View at Google Scholar · View at Scopus
  46. S. S. Seong, C. B. Choi, H. R. Yun, Y. J. Kim, Y. K. Sung, and S. C. Bae, “Effect of lower dose intravenous cyclophosphamide on remission induction in Korean patients with lupus nephritis,” Rheumatology International, vol. 28, no. 5, pp. 453–458, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. K. Takada, M. Arefayene, Z. Desta et al., “Cytochrome P450 pharmacogenetics as a predictor of toxicity and clinical response to pulse cyclophosphamide in lupus nephritis,” Arthritis and Rheumatism, vol. 50, no. 7, pp. 2202–2210, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. M. B. Urowitz, D. Ibañez, Y. Ali, and D. D. Gladman, “Outcomes in patients with active lupus nephritis requiring immunosuppressives who never received cyclophosphamide,” Journal of Rheumatology, vol. 34, no. 7, pp. 1491–1496, 2007. View at Google Scholar · View at Scopus
  49. X. Velásquez, U. Verdejo, L. Massardo et al., “Outcome of Chilean patients with lupus nephritis and response to intravenous cyclophosphamide,” Journal of Clinical Rheumatology, vol. 9, no. 1, pp. 7–14, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. H. Y. Wang, T. G. Cui, F. F. Hou et al., “Induction treatment of proliferative lupus nephritis with leflunomide combined with prednisone: a prospective multi-centre observational study,” Lupus, vol. 17, no. 7, pp. 638–644, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. F. Conti, R. Priori, C. Alessandri, F. R. Spinelli, E. Medda, and G. Valesini, “Safety profile and causes of withdrawal due to adverse events in systemic lupus erythematosus patients treated long-term with cyclosporine A,” Lupus, vol. 9, no. 9, pp. 676–680, 2000. View at Publisher · View at Google Scholar · View at Scopus
  52. T. M. Chan, K. C. Tse, C. S. O. Tang, M. Y. Mok, and F. K. Li, “Long-term study of mycophenolate mofetil as continuous induction and maintenance treatment for diffuse proliferative lupus nephritis,” Journal of the American Society of Nephrology, vol. 16, no. 4, pp. 1076–1084, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. Y. Kipen, G. O. Littlejohn, and E. F. Morand, “Methotrexate use in systemic lupus erythematosus,” Lupus, vol. 6, no. 4, pp. 385–389, 1997. View at Google Scholar · View at Scopus
  54. P. Rahman, S. Humphret-Murto, D. D. Gladman, and M. B. Urowitz, “Cytotoxic therapy in systemic lupus erythematosus: experience from a single center,” Medicine, vol. 76, no. 6, pp. 432–437, 1997. View at Publisher · View at Google Scholar · View at Scopus
  55. F. Goldblatt, S. Chambers, A. Rahman, and D. A. Isenberg, “Serious infections in British patients with systemic lupus erythematosus: hospitalisations and mortality,” Lupus, vol. 18, no. 8, pp. 682–689, 2009. View at Publisher · View at Google Scholar · View at Scopus
  56. B. Zhu, N. Chen, Y. Lin et al., “Mycophenolate mofetil in induction and maintenance therapy of severe lupus nephritis: a meta-analysis of randomized controlled trials,” Nephrology Dialysis Transplantation, vol. 22, no. 7, pp. 1933–1942, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Walsh and D. Jayne, “Rituximab in the treatment of anti-neutrophil cytoplasm antibody associated vasculitis and systemic lupus erythematosus: past, present and future,” Kidney International, vol. 72, no. 6, pp. 676–682, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. C. C. Mok, K. Y. Ying, C. W. Yim, W. L. Ng, and W. S. Wong, “Very long-term outcome of pure lupus membranous nephropathy treated with glucocorticoid and azathioprine,” Lupus, vol. 18, no. 12, pp. 1091–1095, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. M. A. Dooley, D. Jayne, E. M. Ginzler et al., “Mycophenolate versus azathioprine as maintenance therapy for lupus nephritis,” The New England Journal of Medicine, vol. 365, no. 20, pp. 1886–1895, 2011. View at Google Scholar
  60. M. Gayed, S. Bernatsky, R. Ramsey-Goldman, A. E. Clarke, and C. Gordon, “Lupus and cancer,” Lupus, vol. 18, no. 6, pp. 479–485, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. D. D. Gladman, F. Hussain, D. Ibañez, and M. B. Urowitz, “The nature and outcome of infection in systemic lupus erythematosus,” Lupus, vol. 11, no. 4, pp. 234–239, 2002. View at Publisher · View at Google Scholar · View at Scopus
  62. V. Noël, O. Lortholary, P. Casassus et al., “Risk factors and prognostic influence of infection in a single cohort of 87 adults with systemic lupus erythematosus,” Annals of the Rheumatic Diseases, vol. 60, no. 12, pp. 1141–1144, 2001. View at Publisher · View at Google Scholar · View at Scopus
  63. A. Pani, “Standard immunosuppresive therapy of immune-mediated glomerular diseases,” Autoimmunity Reviews, 2012. View at Publisher · View at Google Scholar
  64. D. Roccatello, “Novel diagnostic approaches and cost-benefit balance of treatment of immune-mediated and rare disease in the era of biologic drugs: lessons from the 15th Turin Congress on Immune Pathology and Orphan Disease,” Autoimmunity Reviews, 2012. View at Publisher · View at Google Scholar
  65. G. Leardini and C. Rigon, “The impact of the profile of biologics on treatment costs,” Autoimmunity Reviews, 2012. View at Publisher · View at Google Scholar