1932

Abstract

Systemic lupus erythematosus (SLE) is a devastating autoimmune disease that can result in substantial morbidity and mortality. Diagnosis and treatment of SLE are clinical challenges. Patient presentation and response to therapy are heterogeneous because of the complex immune dysregulation that results in SLE disease pathogenesis. An intricate interplay between genetic risk and skewing of adaptive and innate immune system responses leads to overproduction of type I interferons and other cytokines, complement activation, immune-complex deposition, and ultimately inflammation and tissue damage. Here, we review the classification criteria as well as standard and emerging diagnostic tools available to identify patients with SLE. We then focus on medical management, including novel therapeutics, nonpharmacologic interventions, and comorbidity management.

Keyword(s): biologicinterferonlupustherapies

[Erratum, Closure]

An erratum has been published for this article:
Corrigendum: Systemic Lupus Erythematosus: New Diagnostic and Therapeutic Approaches
Loading

Article metrics loading...

/content/journals/10.1146/annurev-med-043021-032611
2023-01-27
2024-04-28
Loading full text...

Full text loading...

/deliver/fulltext/med/74/1/annurev-med-043021-032611.html?itemId=/content/journals/10.1146/annurev-med-043021-032611&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Sirobhushanam S, Lazar S, Kahlenberg JM. 2021. Interferons in systemic lupus erythematosus. Rheum. Dis. Clin. North Am. 47:297–315
    [Google Scholar]
  2. 2.
    Arbuckle MR, McClain MT, Rubertone MV et al. 2003. Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N. Engl. J. Med. 349:1526–33
    [Google Scholar]
  3. 3.
    Rees F, Doherty M, Lanyon P et al. 2017. Early clinical features in systemic lupus erythematosus: Can they be used to achieve earlier diagnosis? A risk prediction model. Arthritis Care Res. 69:833–41
    [Google Scholar]
  4. 4.
    Drenkard C, Lim SS. 2019. Update on lupus epidemiology: advancing health disparities research through the study of minority populations. Curr. Opin. Rheumatol. 31:689–96
    [Google Scholar]
  5. 5.
    Chan EK, Damoiseaux J, de Melo Cruvinel W et al. 2016. Report on the second International Consensus on ANA Pattern (ICAP) workshop in Dresden; 2015. Lupus 25:797–804
    [Google Scholar]
  6. 6.
    Pisetsky DS. 2017. Antinuclear antibody testing—misunderstood or misbegotten?. Nat. Rev. Rheumatol. 13:495–502
    [Google Scholar]
  7. 7.
    Agmon-Levin N, Damoiseaux J, Kallenberg C et al. 2014. International recommendations for the assessment of autoantibodies to cellular antigens referred to as anti-nuclear antibodies. Ann. Rheum. Dis. 73:17–23
    [Google Scholar]
  8. 8.
    Satoh M, Chan EK, Ho LA et al. 2012. Prevalence and sociodemographic correlates of antinuclear antibodies in the United States. Arthritis Rheum 64:2319–27
    [Google Scholar]
  9. 9.
    Abeles AM, Abeles M. 2013. The clinical utility of a positive antinuclear antibody test result. Am. J. Med. 126:342–48
    [Google Scholar]
  10. 10.
    Li QZ, Karp DR, Quan J et al. 2011. Risk factors for ANA positivity in healthy persons. Arthritis Res. Ther. 13:R38
    [Google Scholar]
  11. 11.
    Mahler M, Hanly JG, Fritzler MJ. 2012. Importance of the dense fine speckled pattern on HEp-2 cells and anti-DFS70 antibodies for the diagnosis of systemic autoimmune diseases. Autoimmun. Rev. 11:642–45
    [Google Scholar]
  12. 12.
    Mariz HA, Sato EI, Barbosa SH et al. 2011. Pattern on the antinuclear antibody-HEp-2 test is a critical parameter for discriminating antinuclear antibody-positive healthy individuals and patients with autoimmune rheumatic diseases. Arthritis Rheum 63:191–200
    [Google Scholar]
  13. 13.
    Pisetsky DS. 2016. Anti-DNA antibodies—quintessential biomarkers of SLE. Nat. Rev. Rheumatol. 12:102–10
    [Google Scholar]
  14. 14.
    Damoiseaux J, Andrade LEC, Carballo OG et al. 2019. Clinical relevance of HEp-2 indirect immunofluorescent patterns: the International Consensus on ANA Patterns (ICAP) perspective. Ann. Rheum. Dis. 78:879–89
    [Google Scholar]
  15. 15.
    Aringer M, Costenbader K, Daikh D et al. 2019. 2019 European League Against Rheumatism/American College of Rheumatology classification criteria for systemic lupus erythematosus. Arthritis Rheumatol 71:1400–12
    [Google Scholar]
  16. 16.
    Suda M, Kishimoto M, Ohde S, Okada M. 2020. Validation of the 2019 ACR/EULAR classification criteria of systemic lupus erythematosus in 100 Japanese patients: a real-world setting analysis. Clin. Rheumatol. 39:1823–27
    [Google Scholar]
  17. 17.
    Abdwani R, Al Masroori E, Abdullah E et al. 2021. Evaluating the performance of ACR, SLICC and EULAR/ACR classification criteria in childhood onset systemic lupus erythematosus. Pediatr. Rheumatol. 19:141
    [Google Scholar]
  18. 18.
    Alexander RV, Rey DS, Conklin J et al. 2021. A multianalyte assay panel with cell-bound complement activation products demonstrates clinical utility in systemic lupus erythematosus. Lupus Sci. Med. 8:e000528
    [Google Scholar]
  19. 19.
    Putterman C, Furie R, Ramsey-Goldman R et al. 2014. Cell-bound complement activation products in systemic lupus erythematosus: comparison with anti-double-stranded DNA and standard complement measurements. Lupus Sci. Med. 1:e000056
    [Google Scholar]
  20. 20.
    Hui-Yuen JS, Gartshteyn Y, Ma M et al. 2018. Cell-bound complement activation products (CB-CAPs) have high sensitivity and specificity in pediatric-onset systemic lupus erythematosus and correlate with disease activity. Lupus 27:2262–68
    [Google Scholar]
  21. 21.
    Ramsey-Goldman R, Alexander RV, Massarotti EM et al. 2020. Complement activation in patients with probable systemic lupus erythematosus and ability to predict progression to American College of Rheumatology-classified systemic lupus erythematosus. Arthritis Rheumatol 72:78–88
    [Google Scholar]
  22. 22.
    Arriens C, Alexander RV, Narain S et al. 2020. Cell-bound complement activation products associate with lupus severity in SLE. Lupus Sci. Med. 7:e000377
    [Google Scholar]
  23. 23.
    Munroe ME, Lu R, Zhao YD et al. 2016. Altered type II interferon precedes autoantibody accrual and elevated type I interferon activity prior to systemic lupus erythematosus classification. Ann. Rheum. Dis. 75:2014–21
    [Google Scholar]
  24. 24.
    Li QZ, Zhou J, Lian Y et al. 2010. Interferon signature gene expression is correlated with autoantibody profiles in patients with incomplete lupus syndromes. Clin. Exp. Immunol. 159:281–91
    [Google Scholar]
  25. 25.
    Fanouriakis A, Kostopoulou M, Alunno A et al. 2019. 2019 Update of the EULAR recommendations for the management of systemic lupus erythematosus. Ann. Rheum. Dis. 78:736–45
    [Google Scholar]
  26. 26.
    Dima A, Jurcut C, Chasset F et al. 2022. Hydroxychloroquine in systemic lupus erythematosus: overview of current knowledge. Ther. Adv. Musculoskelet. Dis. 14:1759720X211073001
    [Google Scholar]
  27. 27.
    Almeida-Brasil CC, Hanly JG, Urowitz M et al. 2022. Flares after hydroxychloroquine reduction or discontinuation: results from the Systemic Lupus International Collaborating Clinics (SLICC) inception cohort. Ann. Rheumat. Dis. 81:370–78
    [Google Scholar]
  28. 28.
    Shinjo SK, Bonfá E, Wojdyla D et al. 2010. Antimalarial treatment may have a time-dependent effect on lupus survival: data from a multinational Latin American inception cohort. Arthritis Rheum 62:855–62
    [Google Scholar]
  29. 29.
    Petri M, Konig MF, Li J, Goldman DW. 2021. Association of higher hydroxychloroquine blood levels with reduced thrombosis risk in systemic lupus erythematosus. Arthritis Rheumatol 73:997–1004
    [Google Scholar]
  30. 30.
    Shipman WD, Vernice NA, Demetres M, Jorizzo JL. 2020. An update on the use of hydroxychloroquine in cutaneous lupus erythematosus: a systematic review. J. Am. Acad. Dermatol. 82:709–22
    [Google Scholar]
  31. 31.
    Lambers WM, Westra J, Bootsma H, de Leeuw K. 2021. Hydroxychloroquine suppresses interferon-inducible genes and B cell activating factor in patients with incomplete and new-onset systemic lupus erythematosus. J. Rheumatol. 48:847–51
    [Google Scholar]
  32. 32.
    Olsen NJ, McAloose C, Carter J et al. 2016. Clinical and immunologic profiles in incomplete lupus erythematosus and improvement with hydroxychloroquine treatment. Autoimmune Dis 2016:8791629
    [Google Scholar]
  33. 33.
    Balevic SJ, Weiner D, Clowse MEB et al. 2022. Hydroxychloroquine PK and exposure-response in pregnancies with lupus: the importance of adherence for neonatal outcomes. Lupus Sci. Med. 9:e000602
    [Google Scholar]
  34. 34.
    Izmirly P, Kim M, Friedman DM et al. 2020. Hydroxychloroquine to prevent recurrent congenital heart block in fetuses of anti-SSA/Ro-positive mothers. J. Am. Coll. Cardiol. 76:292–302
    [Google Scholar]
  35. 35.
    Rosenbaum JT, Costenbader KH, Desmarais J et al. 2021. American College of Rheumatology, American Academy of Dermatology, Rheumatologic Dermatology Society, and American Academy of Ophthalmology 2020 joint statement on hydroxychloroquine use with respect to retinal toxicity. Arthritis Rheumatol 73:908–11
    [Google Scholar]
  36. 36.
    Petri M, Elkhalifa M, Li J et al. 2020. Hydroxychloroquine blood levels predict hydroxychloroquine retinopathy. Arthritis Rheumatol 72:448–53
    [Google Scholar]
  37. 37.
    Illei GG, Austin HA, Crane M et al. 2001. Combination therapy with pulse cyclophosphamide plus pulse methylprednisolone improves long-term renal outcome without adding toxicity in patients with lupus nephritis. Ann. Intern. Med. 135:248–57
    [Google Scholar]
  38. 38.
    Ugarte-Gil MF, Mak A, Leong J et al. 2021. Impact of glucocorticoids on the incidence of lupus-related major organ damage: a systematic literature review and meta-regression analysis of longitudinal observational studies. Lupus Sci. Med. 8:e000590
    [Google Scholar]
  39. 39.
    Apostolopoulos D, Kandane-Rathnayake R, Louthrenoo W et al. 2020. Factors associated with damage accrual in patients with systemic lupus erythematosus with no clinical or serological disease activity: a multicentre cohort study. Lancet Rheumatol 2:e24–e30
    [Google Scholar]
  40. 40.
    Borucki R, Werth VP. 2020. Expert perspective: an evidence-based approach to refractory cutaneous lupus erythematosus. Arthritis Rheumatol 72:1777–85
    [Google Scholar]
  41. 41.
    Sakthiswary R, Suresh E. 2014. Methotrexate in systemic lupus erythematosus: a systematic review of its efficacy. Lupus 23:225–35
    [Google Scholar]
  42. 42.
    Carrión-Barberà I, Polino L, Mejía-Torres M et al. 2022. Leflunomide: a safe and effective alternative in systemic lupus erythematosus. Autoimmun. Rev. 21:102960
    [Google Scholar]
  43. 43.
    Olivieri G, Ceccarelli F, Natalucci F et al. 2021. Five-years drug survival of mycophenolate mofetil therapy in patients with systemic lupus erythematosus: comparison between renal and non-renal involvement. Joint Bone Spine 88:105246
    [Google Scholar]
  44. 44.
    McCune WJ, Golbus J, Zeldes W et al. 1988. Clinical and immunologic effects of monthly administration of intravenous cyclophosphamide in severe systemic lupus erythematosus. N. Engl. J. Med. 318:1423–31
    [Google Scholar]
  45. 45.
    Houssiau FA, Vasconcelos C, D'Cruz D et al. 2002. Immunosuppressive therapy in lupus nephritis: the Euro-Lupus Nephritis Trial, a randomized trial of low-dose versus high-dose intravenous cyclophosphamide. Arthritis Rheum 46:2121–31
    [Google Scholar]
  46. 46.
    Askanase AD, Byron M, Keyes-Elstein LL et al. (ACCESS Trial Group). 2014. Treatment of lupus nephritis with abatacept: the Abatacept and Cyclophosphamide Combination Efficacy and Safety Study. Arthritis Rheumatol 66:3096–104
    [Google Scholar]
  47. 47.
    Appel GB, Contreras G, Dooley MA et al. 2009. Mycophenolate mofetil versus cyclophosphamide for induction treatment of lupus nephritis. J. Am. Soc. Nephrol. 20:1103–12
    [Google Scholar]
  48. 48.
    Furie R, Rovin BH, Houssiau F et al. 2020. Two-year, randomized, controlled trial of belimumab in lupus nephritis. N. Engl. J. Med. 383:1117–28
    [Google Scholar]
  49. 49.
    Park DJ, Kang JH, Lee KE et al. 2019. Efficacy and safety of mycophenolate mofetil and tacrolimus combination therapy in patients with lupus nephritis: a nationwide multicentre study. Clin. Exp. Rheumatol. 37:89–96
    [Google Scholar]
  50. 50.
    Rovin BH, Teng YKO, Ginzler EM et al. 2021. Efficacy and safety of voclosporin versus placebo for lupus nephritis (AURORA 1): a double-blind, randomised, multicentre, placebo-controlled, phase 3 trial. Lancet 397:2070–80
    [Google Scholar]
  51. 51.
    Mok CC, Ho LY, Ying SKY et al. 2020. Long-term outcome of a randomised controlled trial comparing tacrolimus with mycophenolate mofetil as induction therapy for active lupus nephritis. Ann. Rheum. Dis. 79:1070–76
    [Google Scholar]
  52. 52.
    Navarra SV, Guzmán RM, Gallacher AE et al. 2011. Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebo-controlled, phase 3 trial. Lancet 377:721–31
    [Google Scholar]
  53. 53.
    Furie R, Petri M, Zamani O et al. 2011. 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 63:3918–30
    [Google Scholar]
  54. 54.
    Zhang F, Bae SC, Bass D et al. 2018. 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. 77:355–63
    [Google Scholar]
  55. 55.
    Stohl W, Schwarting A, Okada M et al. 2017. Efficacy and safety of subcutaneous belimumab in systemic lupus erythematosus: a fifty-two-week randomized, double-blind, placebo-controlled study. Arthritis Rheumatol 69:1016–27
    [Google Scholar]
  56. 56.
    Singh JA, Shah NP, Mudano AS. 2021. Belimumab for systemic lupus erythematosus. Cochrane Database Syst. Rev. 2:CD010668
    [Google Scholar]
  57. 57.
    Strand V, Berry P, Lin X et al. 2019. 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. 71:829–38
    [Google Scholar]
  58. 58.
    Furie R, Rovin BH, Houssiau F et al. 2020. Two-year, randomized, controlled trial of belimumab in lupus nephritis. N. Engl. J. Med. 383:1117–28
    [Google Scholar]
  59. 59.
    Leandro MJ, Cambridge G, Edwards JC et al. 2005. B-cell depletion in the treatment of patients with systemic lupus erythematosus: a longitudinal analysis of 24 patients. Rheumatology 44:1542–45
    [Google Scholar]
  60. 60.
    Lu TY, Ng KP, Cambridge G et al. 2009. A retrospective seven-year analysis of the use of B cell depletion therapy in systemic lupus erythematosus at University College London Hospital: the first fifty patients. Arthritis Rheum 61:482–87
    [Google Scholar]
  61. 61.
    Merrill JT, Neuwelt CM, Wallace DJ et al. 2010. Efficacy and safety of rituximab in moderately-to-severely active systemic lupus erythematosus: the randomized, double-blind, phase II/III Systemic Lupus Erythematosus Evaluation of Rituximab trial. Arthritis Rheum 62:222–33
    [Google Scholar]
  62. 62.
    Rovin BH, Furie R, Latinis K et al. 2012. Efficacy and safety of rituximab in patients with active proliferative lupus nephritis: the Lupus Nephritis Assessment with Rituximab study. Arthritis Rheum 64:1215–26
    [Google Scholar]
  63. 63.
    Riggs JM, Hanna RN, Rajan B et al. 2018. Characterisation of anifrolumab, a fully human anti-interferon receptor antagonist antibody for the treatment of systemic lupus erythematosus. Lupus Sci. Med. 5:e000261
    [Google Scholar]
  64. 64.
    Furie R, Khamashta M, Merrill JT et al. 2017. Anifrolumab, an anti-interferon-α receptor monoclonal antibody, in moderate-to-severe systemic lupus erythematosus. Arthritis Rheumatol 69:376–86
    [Google Scholar]
  65. 65.
    Furie RA, Morand EF, Bruce IN et al. 2019. Type I interferon inhibitor anifrolumab in active systemic lupus erythematosus (TULIP-1): a randomised, controlled, phase 3 trial. Lancet Rheumatol 1:e208–e219
    [Google Scholar]
  66. 66.
    Morand EF, Furie R, Tanaka Y et al. 2020. Trial of anifrolumab in active systemic lupus erythematosus. N. Engl. J. Med. 382:211–21
    [Google Scholar]
  67. 67.
    Furie R, Morand EF, Askanase AD et al. 2021. Anifrolumab reduces flare rates in patients with moderate to severe systemic lupus erythematosus. Lupus 30:1254–63
    [Google Scholar]
  68. 68.
    Heo YA. 2021. Voclosporin: first approval. Drugs 81:605–10
    [Google Scholar]
  69. 69.
    Rovin BH, Solomons N, Pendergraft WF et al. 2019. A randomized, controlled double-blind study comparing the efficacy and safety of dose-ranging voclosporin with placebo in achieving remission in patients with active lupus nephritis. Kidney Int 95:219–31
    [Google Scholar]
  70. 70.
    Saxena A, Mela C, Coeshall A. 2021. Voclosporin for lupus nephritis: interim analysis of the AURORA 2 extension study. Arthritis Rheumatol 73:Suppl. 101425 (Abstr.)
    [Google Scholar]
  71. 71.
    Mok CC. 2019. The Jakinibs in systemic lupus erythematosus: progress and prospects. Expert Opin. Investig. Drugs 28:85–92
    [Google Scholar]
  72. 72.
    Furie R, Werth VP, Merola JF et al. 2019. Monoclonal antibody targeting BDCA2 ameliorates skin lesions in systemic lupus erythematosus. J. Clin. Investig. 129:1359–71
    [Google Scholar]
  73. 73.
    Robinson S, Thomas R. 2021. Potential for antigen-specific tolerizing immunotherapy in systematic lupus erythematosus. Front. Immunol. 12:654701
    [Google Scholar]
  74. 74.
    Ruiz-Irastorza G, Egurbide MV, Olivares N et al. 2008. Vitamin D deficiency in systemic lupus erythematosus: prevalence, predictors and clinical consequences. Rheumatology 47:920–23
    [Google Scholar]
  75. 75.
    Mok CC. 2013. Vitamin D and systemic lupus erythematosus: an update. Expert Rev. Clin. Immunol. 9:453–63
    [Google Scholar]
  76. 76.
    Lima GL, Paupitz J, Aikawa NE et al. 2016. Vitamin D supplementation in adolescents and young adults with juvenile systemic lupus erythematosus for improvement in disease activity and fatigue scores: a randomized, double-blind, placebo-controlled trial. Arthritis Care Res. 68:91–98
    [Google Scholar]
  77. 77.
    Piantoni S, Andreoli L, Allegri F et al. 2012. Low levels of vitamin D are common in primary antiphospholipid syndrome with thrombotic disease. Reumatismo 64:307–13
    [Google Scholar]
  78. 78.
    Andreoli L, Piantoni S, Dall'Ara F et al. 2012. Vitamin D and antiphospholipid syndrome. Lupus 21:736–40
    [Google Scholar]
  79. 79.
    Petri M, Bello KJ, Fang H, Magder LS. 2013. Vitamin D in systemic lupus erythematosus: modest association with disease activity and the urine protein-to-creatinine ratio. Arthritis Rheum 65:1865–71
    [Google Scholar]
  80. 80.
    Athanassiou L, Kostoglou-Athanassiou I, Tsakiridis P et al. 2022. Vitamin D levels in Greek patients with systemic lupus erythematosus. Lupus 31:125–32
    [Google Scholar]
  81. 81.
    Fava A, Petri M. 2019. Systemic lupus erythematosus: diagnosis and clinical management. J. Autoimmun. 96:1–13
    [Google Scholar]
  82. 82.
    van der Meulen TA, Harmsen HJM, Vila AV et al. 2019. Shared gut, but distinct oral microbiota composition in primary Sjögren's syndrome and systemic lupus erythematosus. J. Autoimmun. 97:77–87
    [Google Scholar]
  83. 83.
    Hevia A, Milani C, López P et al. 2014. Intestinal dysbiosis associated with systemic lupus erythematosus. mBio 5:e01548–14
    [Google Scholar]
  84. 84.
    Yamamoto EA, Jørgensen TN. 2019. Relationships between vitamin D, gut microbiome, and systemic autoimmunity. Front. Immunol. 10:3141
    [Google Scholar]
  85. 85.
    Zegarra-Ruiz DF, El Beidaq A, Iniguez AJ et al. 2019. A diet-sensitive commensal lactobacillus strain mediates TLR7-dependent systemic autoimmunity. Cell Host Microbe 25:113–27.e6
    [Google Scholar]
  86. 86.
    Mu Q, Tavella VJ, Kirby JL et al. 2017. Antibiotics ameliorate lupus-like symptoms in mice. Sci. Rep. 7:13675
    [Google Scholar]
  87. 87.
    Pocovi-Gerardino G, Correa-Rodríguez M, Callejas-Rubio JL et al. 2021. Beneficial effect of Mediterranean diet on disease activity and cardiovascular risk in systemic lupus erythematosus patients: a cross-sectional study. Rheumatology 60:160–69
    [Google Scholar]
  88. 88.
    Charoenwoodhipong P, Harlow SD, Marder W et al. 2020. Dietary omega polyunsaturated fatty acid intake and patient-reported outcomes in systemic lupus erythematosus: the Michigan lupus epidemiology and surveillance program. Arthritis Care Res. 72:874–81
    [Google Scholar]
  89. 89.
    Zamansky GB. 1985. Sunlight-induced pathogenesis in systemic lupus erythematosus. J. Investig. Dermatol. 85:179–80
    [Google Scholar]
  90. 90.
    Stege H, Budde MA, Grether-Beck S, Krutmann J 2000. Evaluation of the capacity of sunscreens to photoprotect lupus erythematosus patients by employing the photoprovocation test. Photodermatol. Photoimmunol. Photomed. 16:256–59
    [Google Scholar]
  91. 91.
    Estadt SN, Maz MP, Musai J, Kahlenberg JM. 2022. Mechanisms of photosensitivity in autoimmunity. J. Investig. Dermatol. 142:849–56
    [Google Scholar]
  92. 92.
    Kuhn A, Gensch K, Haust M et al. 2011. Photoprotective effects of a broad-spectrum sunscreen in ultraviolet-induced cutaneous lupus erythematosus: a randomized, vehicle-controlled, double-blind study. J. Am. Acad. Dermatol. 64:37–48
    [Google Scholar]
  93. 93.
    Abdul Kadir WD, Jamil A, Shaharir SS et al. 2018. Photoprotection awareness and practices among patients with systemic lupus erythematosus and its association with disease activity and severity. Lupus 27:1287–95
    [Google Scholar]
  94. 94.
    Al Sawah S, Zhang X, Zhu B et al. 2015. Effect of corticosteroid use by dose on the risk of developing organ damage over time in systemic lupus erythematosus—the Hopkins Lupus Cohort. Lupus Sci. Med. 2:e000066
    [Google Scholar]
  95. 95.
    Thamer M, Hernán MA, Zhang Y et al. 2009. Prednisone, lupus activity, and permanent organ damage. J. Rheumatol. 36:560–64
    [Google Scholar]
  96. 96.
    Gladman DD, Urowitz MB, Rahman P et al. 2003. Accrual of organ damage over time in patients with systemic lupus erythematosus. J. Rheumatol. 30:1955–59
    [Google Scholar]
  97. 97.
    Condon MB, Ashby D, Pepper RJ et al. 2013. 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. 72:1280–86
    [Google Scholar]
  98. 98.
    Barber MRW, Drenkard C, Falasinnu T et al. 2021. Global epidemiology of systemic lupus erythematosus. Nat. Rev. Rheumatol. 17:515–32
    [Google Scholar]
  99. 99.
    Gandelman JS, Khan OA, Shuey MM et al. 2020. Increased incidence of resistant hypertension in patients with systemic lupus erythematosus: a retrospective cohort study. Arthritis Care Res. 72:534–43
    [Google Scholar]
  100. 100.
    Singh RR, Yen EY 2018. SLE mortality remains disproportionately high, despite improvements over the last decade. Lupus 27:1577–81
    [Google Scholar]
  101. 101.
    Martz CD, Allen AM, Fuller-Rowell TE et al. 2019. Vicarious racism stress and disease activity: the Black Women's Experiences Living with Lupus (BeWELL) study. J. Racial Ethn. Health Disparities 6:1044–51
    [Google Scholar]
  102. 102.
    Minhas D, Marder W, Harlow S et al. 2021. Access and cost-related nonadherence to prescription medications among lupus patients and controls: the Michigan Lupus Epidemiology and Surveillance program. Arthritis Care Res. 73:1561–67
    [Google Scholar]
/content/journals/10.1146/annurev-med-043021-032611
Loading
/content/journals/10.1146/annurev-med-043021-032611
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error