410
Views
2
CrossRef citations to date
0
Altmetric
REVIEW

Impact of Belimumab on Patient-Reported Outcomes in Systemic Lupus Erythematosus: Insights from Clinical Trials and Real-World Evidence

ORCID Icon, & ORCID Icon
Pages 1-13 | Received 10 Nov 2022, Accepted 11 Jan 2023, Published online: 19 Jan 2023

References

  • Kaul A, Gordon C, Crow MK, et al. Systemic lupus erythematosus. Nat Rev Dis Primers. 2016;2:16039. doi:10.1038/nrdp.2016.39
  • Nived O, Jonsen A, Bengtsson AA, Bengtsson C, Sturfelt G. High predictive value of the systemic lupus international collaborating clinics/American college of rheumatology damage index for survival in systemic lupus erythematosus. J Rheumatol. 2002;29:1398–1400.
  • Bernatsky S, Boivin JF, Joseph L, et al. Mortality in systemic lupus erythematosus. Arthritis Rheum. 2006;54:2550–2557. doi:10.1002/art.21955
  • Gomez A, Hani Butrus F, Johansson P, et al. Impact of overweight and obesity on patient-reported health-related quality of life in systemic lupus erythematosus. Rheumatology. 2021;60:1260–1272. doi:10.1093/rheumatology/keaa453
  • Parodis I, Studenic P. Patient-reported outcomes in systemic lupus erythematosus. can lupus patients take the driver’s seat in their disease monitoring? J Clin Med. 2022;11(2):340. doi:10.3390/jcm11020340
  • Fanouriakis A, Kostopoulou M, Alunno A, et al. 2019 update of the EULAR recommendations for the management of systemic lupus erythematosus. Ann Rheum Dis. 2019;78:736–745. doi:10.1136/annrheumdis-2019-215089
  • Szelinski F, Lino AC, Dorner T. B cells in systemic lupus erythematosus. Curr Opin Rheumatol. 2022;34:125–132. doi:10.1097/BOR.0000000000000865
  • Parodis I, Stockfelt M, Sjowall C, Cell B. Therapy in systemic lupus erythematosus: from rationale to clinical practice. Front Med. 2020;7:316. doi:10.3389/fmed.2020.00316
  • Navarra SV, Guzman RM, Gallacher AE, et al. Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebo-controlled, Phase 3 trial. Lancet. 2011;377:721–731. doi:10.1016/S0140-6736(10)61354-2
  • Furie R, Petri M, Zamani O, 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. 2011;63:3918–3930. doi:10.1002/art.30613
  • Stohl W, Schwarting A, Okada M, et al. Efficacy and safety of subcutaneous belimumab in systemic lupus erythematosus: a fifty-two-week randomized, double-blind, placebo-controlled study. Arthritis Rheumatol. 2017;69:1016–1027. doi:10.1002/art.40049
  • Brunner HI, Abud-Mendoza C, Viola DO, et al. Paediatric Rheumatology International Trials and G; the Pediatric Rheumatology Collaborative Study, Safety and efficacy of intravenous belimumab in children with systemic lupus erythematosus: results from a randomised, placebo-controlled trial. Ann Rheum Dis. 2020;79:1340–1348. doi:10.1136/annrheumdis-2020-217101
  • Furie R, Rovin BH, Houssiau F, et al. Two-year, randomized, controlled trial of belimumab in lupus nephritis. NEJM. 2020;383:1117–1128. doi:10.1056/NEJMoa2001180
  • van Vollenhoven RF, Petri MA, Cervera R, et al. Belimumab in the treatment of systemic lupus erythematosus: high disease activity predictors of response. Ann Rheum Dis. 2012;71:1343–1349. doi:10.1136/annrheumdis-2011-200937
  • Parodis I, Sjowall C, Jonsen A, et al. Smoking and pre-existing organ damage reduce the efficacy of belimumab in systemic lupus erythematosus. Autoimmun Rev. 2017;16:343–351. doi:10.1016/j.autrev.2017.02.005
  • Parodis I, Gomez A, Frodlund M, et al. Smoking reduces the efficacy of belimumab in mucocutaneous lupus. Expert Opin Biol Ther. 2018;18:911–920. doi:10.1080/14712598.2018.1494719
  • Ramskold D, Parodis I, Lakshmikanth T, et al. B cell alterations during BAFF inhibition with belimumab in SLE. EBioMedicine. 2019;40:517–527. doi:10.1016/j.ebiom.2018.12.035
  • Parodis I, Åkerström E, Sjöwall C, et al. Autoantibody and cytokine profiles during treatment with belimumab in patients with systemic lupus erythematosus. Int J Mol Sci. 2020;21(10):3463. doi:10.3390/ijms21103463
  • Gatto M, Saccon F, Zen M, et al. Early disease and low baseline damage as predictors of response to belimumab in patients with systemic lupus erythematosus in a real-life setting. Arthritis Rheumatol. 2020;72:1314–1324. doi:10.1002/art.41253
  • Gatto M, Saccon F, Andreoli L, et al. Durable renal response and safety with add-on belimumab in patients with lupus nephritis in real-life setting (BeRLiSS-LN). Results from a large, nationwide, multicentric cohort. J Autoimmun. 2021;124:102729. doi:10.1016/j.jaut.2021.102729
  • Wallace DJ, Ginzler EM, Merrill JT, et al. Safety and efficacy of belimumab plus standard therapy for up to thirteen years in patients with systemic lupus erythematosus. Arthritis Rheumatol. 2019;71:1125–1134. doi:10.1002/art.40861
  • Tanaka Y, Bae SC, Bass D, et al. Long-term open-label continuation study of the safety and efficacy of belimumab for up to 7 years in patients with systemic lupus erythematosus from Japan and South Korea. RMD Open. 2021;7:07. doi:10.1136/rmdopen-2021-001629
  • Collins CE, Cortes-Hernandez J, Garcia MA, et al. Real-world effectiveness of belimumab in the treatment of systemic lupus erythematosus: pooled analysis of multi-country data from the OBSErve Studies. Rheumatol Ther. 2020;7:949–965. doi:10.1007/s40744-020-00243-2
  • Fanouriakis A, Adamichou C, Koutsoviti S, et al. Low disease activity-irrespective of serologic status at baseline-associated with reduction of corticosteroid dose and number of flares in patients with systemic lupus erythematosus treated with belimumab: a real-life observational study. Semin Arthritis Rheum. 2018;48:467–474. doi:10.1016/j.semarthrit.2018.02.014
  • Iaccarino L, Andreoli L, Bocci EB, et al. Clinical predictors of response and discontinuation of belimumab in patients with systemic lupus erythematosus in real life setting. Results of a large, multicentric, nationwide study. J Autoimmun. 2018;86:1–8. doi:10.1016/j.jaut.2017.09.004
  • Sheikh SZ, Scheinberg MA, Wei JCC, et al. Mortality and adverse events of special interest with intravenous belimumab for adults with active, autoantibody-positive systemic lupus erythematosus (BASE): a multicentre, double-blind, randomised, placebo-controlled, Phase 4 trial. Lancet Rheumatol. 2021;3:E122–E130. doi:10.1016/S2665-9913(20)30355-6
  • Xie W, Huang H, Zhan S, Zhang Z. Risk of psychiatric disorders and all-cause mortality with belimumab therapy in patients with systemic lupus erythematosus: a meta-analysis of randomised controlled trials. Lupus Sci Med. 2021;8(1):e000534. doi:10.1136/lupus-2021-000534
  • Bangert E, Wakani L, Merchant M, Strand V, Touma Z. Impact of belimumab on patient-reported outcomes in systemic lupus erythematosus: review of clinical studies. Patient Relat Outcome Meas. 2019;10:1–7. doi:10.2147/PROM.S134326
  • Gomez A, Parodis I. Do biological agents improve health-related quality of life in patients with systemic lupus erythematosus? Results from a systematic search of the literature. Autoimmun Rev. 2022;21(11):103188. doi:10.1016/j.autrev.2022.103188
  • Ware J, Sherbourne C, The MOS. 36-item short-form health survey (SF-36). I. Conceptual framework and item selection. Med Care. 1992;30:473–483. doi:10.1097/00005650-199206000-00002
  • EuroQol Group. EuroQol--a new facility for the measurement of health-related quality of life. Health Policy. 1990;16:199–208. doi:10.1016/0168-8510(90)90421-9
  • Webster K, Cella D, Yost K. The functional assessment of chronic illness therapy (FACIT) Measurement System: properties, applications, and interpretation. Health Qual Life Outcomes. 2003;1:79. doi:10.1186/1477-7525-1-79
  • EuroQol Research Foundation. EQ-5D-3L user guide; 2018. Available from: https://euroqol.org/publications/user-guides. Accessed July 30, 2020.
  • Wallace DJ, Stohl W, Furie RA, et al. A Phase II, randomized, double-blind, placebo-controlled, dose-ranging study of belimumab in patients with active systemic lupus erythematosus. Arthritis Rheum. 2009;61:1168–1178. doi:10.1002/art.24699
  • Strand V, Levy RA, Cervera R, et al. Study, Improvements in health-related quality of life with belimumab, a B-lymphocyte stimulator-specific inhibitor, in patients with autoantibody-positive systemic lupus erythematosus from the randomised controlled BLISS trials. Ann Rheum Dis. 2014;73:838–844. doi:10.1136/annrheumdis-2012-202865
  • Lindblom J, Gomez A, Borg A, et al. EQ-5D-3L full health state discriminates between drug and placebo in clinical trials of systemic lupus erythematosus. Rheumatology. 2021;60:4703–4716. doi:10.1093/rheumatology/keab080
  • Gomez A, Qiu V, Cederlund A, et al. Adverse health-related quality of life outcome despite adequate clinical response to treatment in systemic lupus erythematosus. Front Med. 2021;8:651249. doi:10.3389/fmed.2021.651249
  • Druce KL, Jones GT, Macfarlane GJ, Basu N. Patients receiving anti-TNF therapies experience clinically important improvements in RA-related fatigue: results from the British Society for Rheumatology Biologics Register for Rheumatoid Arthritis. Rheumatology. 2015;54:964–971. doi:10.1093/rheumatology/keu390
  • Borg A, Gomez A, Cederlund A, et al. Contribution of abnormal BMI to adverse health-related quality of life outcomes after a 52-week therapy in patients with SLE. Rheumatology. 2021;60:4205–4217. doi:10.1093/rheumatology/keaa909
  • Doria A, Stohl W, Schwarting A, et al. Efficacy and safety of subcutaneous belimumab in anti-double-stranded DNA-positive, hypocomplementemic patients with systemic lupus erythematosus. Arthritis Rheumatol. 2018;70:1256–1264. doi:10.1002/art.40511
  • Strand V, Berry P, Lin X, Asukai Y, Punwaney R, Ramachandran S. Long-term impact of belimumab on health-related quality of life and fatigue in patients with systemic lupus erythematosus: six years of treatment. Arthritis Care Res. 2019;71:829–838. doi:10.1002/acr.23788
  • Zhang F, Bae SC, Bass D, et al. A pivotal phase III, randomised, placebo-controlled study of belimumab in patients with systemic lupus erythematosus located in China, Japan and South Korea. Ann Rheum Dis. 2018;77:355–363. doi:10.1136/annrheumdis-2017-211631
  • Ginzler E, Guedes Barbosa LS, D’Cruz D, et al. At the time of the, EMBRACE: phase 3/4, randomized, 52-week study of belimumab efficacy and safety in patients of black African Ancestry With Systemic Lupus Erythematosus. Arthritis Rheumatol. 2021;2021:24.
  • Scheinberg M, Golmia R. Real life experience on the effect of Belimumab in patients with active systemic lupus. Springerplus. 2014;3:758. doi:10.1186/2193-1801-3-758
  • Parodis I, Lopez Benavides AH, Zickert A, et al. The impact of belimumab and rituximab on health-related quality of life in patients with systemic lupus erythematosus. Arthritis Care Res. 2019;71:811–821. doi:10.1002/acr.23718
  • Schwarting A, Mockel T, Lutgendorf F, et al. Fatigue in SLE: diagnostic and pathogenic impact of anti-N-methyl-D-aspartate receptor (NMDAR) autoantibodies. Ann Rheum Dis. 2019;78:1226–1234. doi:10.1136/annrheumdis-2019-215098
  • Touma Z, Sayani A, Pineau CA, et al. Belimumab use, clinical outcomes and glucocorticoid reduction in patients with systemic lupus erythematosus receiving belimumab in clinical practice settings: results from the OBSErve Canada Study. Rheumatol Int. 2017;37:865–873. doi:10.1007/s00296-017-3682-9
  • Schwarting A, Schroeder JO, Alexander T, et al. First real-world insights into belimumab use and outcomes in routine clinical care of systemic lupus erythematosus in Germany: RESULTS FROM the OBSErve Germany Study. Rheumatol Ther. 2016;3:271–290. doi:10.1007/s40744-016-0047-x
  • von Kempis J, Duetsch S, Reuschling N, et al. Clinical outcomes in patients with systemic lupus erythematosus treated with belimumab in clinical practice settings: a retrospective analysis of results from the OBSErve study in Switzerland. Swiss Med Wkly. 2019;149:w20022.
  • van Vollenhoven RF, Mosca M, Bertsias G, et al. Treat-to-target in systemic lupus erythematosus: recommendations from an international task force. Ann Rheum Dis. 2014;73:958–967. doi:10.1136/annrheumdis-2013-205139
  • McElhone K, Abbott J, Shelmerdine J, et al. Development and validation of a disease-specific health-related quality of life measure, the LupusQol, for adults with systemic lupus erythematosus. Arthritis Rheum. 2007;57:972–979. doi:10.1002/art.22881
  • Jolly M, Pickard AS, Block JA, et al. Disease-specific patient reported outcome tools for systemic lupus erythematosus. Semin Arthritis Rheum. 2012;42:56–65. doi:10.1016/j.semarthrit.2011.12.005
  • Izadi Z, Gandrup J, Katz PP, Yazdany J. Patient-reported outcome measures for use in clinical trials of SLE: a review. Lupus Sci Med. 2018;5:e000279. doi:10.1136/lupus-2018-000279
  • Devilliers H, Amoura Z, Besancenot JF, et al. Responsiveness of the 36-item short form health survey and the lupus quality of life questionnaire in SLE. Rheumatology. 2015;54:940–949. doi:10.1093/rheumatology/keu410
  • Singh JA, Shah NP, Mudano AS. Belimumab for systemic lupus erythematosus. Cochrane Database Syst Rev. 2021;2:CD010668. doi:10.1002/14651858.CD010668.pub2
  • Levy RA, Gonzalez-Rivera T, Khamashta M, et al. 10 Years of belimumab experience: what have we learnt? Lupus. 2021;30:1705–1721. doi:10.1177/09612033211028653
  • Furie R, Stohl W, Ginzler EM, 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 Res Ther. 2008;10:R109. doi:10.1186/ar2506
  • Maslen T, Bruce IN, D’Cruz D, et al. Efficacy of belimumab in two serologically distinct high disease activity subgroups of patients with systemic lupus erythematosus: post-hoc analysis of data from the phase III programme. Lupus Sci Med. 2021;8:2. doi:10.1136/lupus-2020-000459
  • Dashiell-Aje E, Harding G, Pascoe K, DeVries J, Berry P, Ramachandran S. Patient evaluation of satisfaction and outcomes with an autoinjector for self-administration of subcutaneous belimumab in patients with systemic lupus erythematosus. Patient. 2018;11:119–129. doi:10.1007/s40271-017-0276-2