Systemic lupus erythematosus

Nature Reviews Disease Primers

Volumn 2, Issue , 2016, Pages

  Kaul, Arvind ^a   Gordon, Caroline ^b   Crow, Mary K ^c   Touma, Zahi ^d   Urowitz, Murray B ^d   Van Vollenhoven, Ronald ^e   Ruiz Irastorza, Guillermo ^f   Hughes, Graham ^g  

^a ST GEORGE S HOSPITAL   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c HOSPITAL FOR SPECIAL SURGERY   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

^e KAROLINSKA INSTITUTE   (Sweden)

^f BIOCRUCES BIZKAIA HEALTH RESEARCH INSTITUTE   (Spain)

^g LONDON BRIDGE HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AZATHIOPRINE; BELIMUMAB; CYCLOPHOSPHAMIDE; CYTOKINE; GLUCOCORTICOID; HYDROXYCHLOROQUINE; MYCOPHENOLATE MOFETIL; RITUXIMAB; IMMUNOSUPPRESSIVE AGENT; MONOCLONAL ANTIBODY;

ADAPTIVE IMMUNITY; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CLINICAL FEATURE; COMORBIDITY; CORTICOSTEROID THERAPY; DISEASE ACTIVITY; DISEASE CLASSIFICATION; DRUG TARGETING; ENVIRONMENTAL FACTOR; EPSTEIN BARR VIRUS INFECTION; GENE INTERACTION; GENETIC HETEROGENEITY; HEREDITY; HUMAN; IMMUNE DYSREGULATION; IMMUNOSUPPRESSIVE TREATMENT; INCIDENCE; INNATE IMMUNITY; LUPUS ERYTHEMATOSUS NEPHRITIS; MACROPHAGE; MAINTENANCE THERAPY; MORTALITY RISK; NONHUMAN; PATHOPHYSIOLOGY; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PREVALENCE; PRIORITY JOURNAL; PROPHYLAXIS; QUALITY OF LIFE; RADIATION EXPOSURE; RANDOMIZED CONTROLLED TRIAL (TOPIC); SCREENING; SYSTEMATIC REVIEW (TOPIC); SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE; ULTRAVIOLET RADIATION; UNSPECIFIED SIDE EFFECT; ADOLESCENT; ADULT; ADVERSE DRUG REACTION; ARTHRALGIA; COMPLICATION; ENDOGENOUS RETROVIRUS; FATIGUE; FEMALE; IMMUNOLOGY; PATHOGENICITY; PSYCHOLOGY; RISK FACTOR; SMOKING;

ADOLESCENT; ADULT; ANTIBODIES, MONOCLONAL, HUMANIZED; ARTHRALGIA; B-LYMPHOCYTES; COMORBIDITY; DRUG-RELATED SIDE EFFECTS AND ADVERSE REACTIONS; ENDOGENOUS RETROVIRUSES; EPSTEIN-BARR VIRUS INFECTIONS; FATIGUE; FEMALE; HUMANS; IMMUNOSUPPRESSIVE AGENTS; LUPUS ERYTHEMATOSUS, SYSTEMIC; QUALITY OF LIFE; RISK FACTORS; SMOKING; T-LYMPHOCYTES; ULTRAVIOLET RAYS;

EID: 85006190192     PISSN: None     EISSN: 2056676X     Source Type: Journal    
DOI: 10.1038/nrdp.2016.39     Document Type: Article

References (216)

1. Faurschou, M., Starklint, H., Halberg, P. & Jacobsen, S. Prognostic factors in lupus nephritis: diagnostic and therapeutic delay increases the risk of terminal renal failure. J. Rheumatol. 33, 1563-1569 (2006).
2. Sullivan, K. E. Genetics of systemic lupus erythematosus: clinical implications. Rheum. Dis. Clin. North Am. 26, 1229-1256 (2000).
3. Moser, K. L., Kelly, J. A., Lessard, C. J. & Harley, J. B. Recent insights into the genetic basis of systemic lupus erythematosus. Genes Immun. 10, 373-379 (2009).
4. Tsokos, G. C. & Kammer, G. M. Molecular aberrations in human systemic lupus erythematosus. Mol. Med. Today 6, 418-424 (2000).
5. Deng, Y. & Tsao, B. Genetic susceptibility to systemic lupus erythematosus in the genomic era. Nat. Rev. Rheumatol. 6, 683-692 (2010).
6. Buyon, J. P. et al. The effect of combined estrogen and progesterone hormone replacement therapy on disease activity in systemic lupus erythematosus: a randomized trial. Ann. Intern. Med. 142, 953-962 (2005).
7. Chang, D. M., Lan, J. L., Lin, H. Y. & Luo, S. F. Dehydroepiandrosterone treatment of women with mild-to-moderate systemic lupus erythematosus: a multicenter randomized, double-blind, placebo-controlled trial. Arthritis Rheum. 46, 2924-2927 (2002).
8. Tektonidou, M. G., Laskari, K., Panagiotakos, D. B. & Moutsopoulos, H. M. Risk factors for thrombosis and primary thrombosis prevention in patients with systemic lupus erythematosus with or without antiphospholipid antibodies. Arthritis Rheum. 61, 2929-2936 (2009).
9. Mok, C. C., Tang, S., To, C. & Petri, M. Incidence and risk factors of thromboembolism in systemic lupus erythematosus: a comparison of three ethnic groups. Arthritis Rheum. 52, 2774-2782 (2005).
10. Mak, A., Cheung, M. W. L., Chiew, H. J., Liu, Y. & Ho, R.C. Global trend of survival and damage of systemic lupus erythematosus: meta-analysis and meta-regression of observational studies from the 1950s to 2000s. Semin. Arthritis Rheum. 41, 2830-2839 (2012).
11. Quismorio, F. P. & Torralba, T. P. in Dubois Lupus Erythematosus and Related Syndromes (eds Wallace, D. J. & Hahn, B. H.) 526-540 (2013).
12. Castrejon, I. et al. Indices to assess patients with systemic lupus erythematosus in clinical trials, long-term observational studies, and clinical care. Clin. Exp. Rheumatol. 32, S585-S595 (2014).
13. Kumar, K., Chambers, S. & Gordon, C. Challenges of ethnicity in SLE. Best. Pract. Res. Clin. Rheumatol. 23, 549-561 (2009).
14. Pons-Estel, G. J., Alarcon, G. S., Scofield, L., Reinlib, L. & Cooper, G. S. Understanding the epidemiology and progression of systemic lupus erythematosus. Semin. Arthritis Rheum. 39, 257-268 (2010).
15. Lim, S. S. et al. The incidence and prevalence of systemic lupus erythematosus, 2002-2004: the Georgia Lupus Registry. Arthritis Rheumatol. 66, 357-368 (2014).
16. Somers, E. C. et al. Population-based incidence and prevalence of systemic lupus erythematosus: the Michigan Lupus Epidemiology and Surveillance program. Arthritis Rheumatol. 66, 369-378 (2014).
17. Laustrup, H., Voss, A., Green, A. & Junker, P. Occurrence of systemic lupus erythematosus in a Danish community: an 8-year prospective study. Scand. J. Rheumatol. 38, 128-132 (2009).
18. Rees, F. et al. The incidence and prevalence of systemic lupus erythematosus in the UK, 1999-2012. Ann. Rheum. Dis. 75, 136-141 (2016).
19. Johnson, A. E., Gordon, C., Palmer, R. G. & Bacon, P. A. The prevalence and incidence of systemic lupus erythematosus in Birmingham, England. Relationship to ethnicity and country of birth. Arthritis Rheum. 38, 551-558 (1995).
20. Yee, C. S. et al. Birmingham SLE cohort: outcomes of a large inception cohort followed for up to 21 years. Rheumatology (Oxford) 54, 836-843 (2015).
21. Sexton, D. J. et al. ESRD from lupus nephritis in the United States, 1995-2010. Clin. J. Am. Soc. Nephrol. 10, 251-259 (2015).
22. Flower, C., Hennis, A. J., Hambleton, I. R., Nicholson, G. D. & Liang, M. H. Systemic lupus erythematosus in an African Caribbean population: incidence, clinical manifestations, and survival in the Barbados National Lupus Registry. Arthritis Care Res. (Hoboken) 64, 1151-1158 (2012).
23. Ferucci, E. D. et al. Prevalence and incidence of systemic lupus erythematosus in a population-based registry of American Indian and Alaska native people, 2007-2009. Arthritis Rheumatol. 66, 2494-2502 (2014).
24. Segasothy, M. & Phillips, P. A. Systemic lupus erythematosus in Aborigines and Caucasians in central Australia: a comparative study. Lupus 10, 2439-2444 (2001).
25. Bossingham, D. Systemic lupus erythematosus in the far north of Queensland. Lupus 12, 327-331 (2003).
26. Yeh, K. W., Yu, C. H., Chan, P. C., Horng, J. T. & Huang, J. L. Burden of systemic lupus erythematosus in Taiwan: a population-based survey. Rheumatol. Int. 33, 1805-1811 (2013).
27. Ju, J. H. et al. Prevalence of systemic lupus erythematosus in South Korea: an administrative database study. J. Epidemiol. 24, 1295-1303 (2014).
28. Shim, J. S., Sung, Y. K., Joo, Y. B., Lee, H. S. & Bae, S. C. Prevalence and incidence of systemic lupus erythematosus in South Korea. Rheumatol. Int. 34, 909-917 (2014).
29. Yurkovich, M., Vostretsova, K., Chen, W. & Avina-Zubieta, J. A. Overall and cause-specific mortality in patients with systemic lupus erythematosus: a meta-analysis of observational studies. Arthritis Care Res. (Hobeken) 66, 608-616 (2014).
30. 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).
31. Gonzalez, L. A., Toloza, S. M. & Alarcon, G. S. Impact of race and ethnicity in the course and outcome of systemic lupus erythematosus. Rheum. Dis. Clin. North Am. 40, 2433-2438 (2014).
32. Gustafsson, J. T. et al. Risk factors for cardiovascular mortality in patients with systemic lupus erythematosus, a prospective cohort study. Arthritis Res. Ther. 14, R46 (2012).
33. Crow, M. K., Olferiev, M. & Kirou, K. A. Targeting of type I interferon in systemic autoimmune diseases. Transl Res. 165, 296-305 (2015).
34. James, J. A. Clinical perspectives on lupus genetics: advances and opportunities. Rheum. Dis. Clin. North Am. 40, 413-432 (2014).
35. Truedsson, L. et al. Complement deficiencies and systemic lupus erythematosus. Autoimmunity 40, 560-566 (2007).
36. Graham, R. R. et al. Specific combinations of HLA-DR2 and DR3 class II haplotypes contribute graded risk for disease susceptibility and autoantibodies in human SLE. Eur. J. Hum. Genet. 15, 823-830 (2007).
37. Price, P. et al. The genetic basis for the association of the 8.1 ancestral haplotype (A1, B8, DR3) with multiple immunopathological diseases. Immunol. Rev. 167, 257-274 (1999).
38. Santer, D. M. et al. C1q deficiency leads to the defective suppression of IFN- in response to nucleoprotein containing immune complexes. J. Immunol. 185, 4738-4749 (2010).
39. Crow, Y. J. & Manel, N. Aicardi-Goutières syndrome and the type I interferonopathies. Nat. Rev. Immunol. 15, 4429-4440 (2015).
40. Namjou, B. et al. Evaluation of the TREX1 gene in a large multi-ancestral lupus cohort. Genes Immun. 12, 270-279 (2011).
41. Niewold, T. B. et al. Association of the IRF5 risk haplotype with high serum interferon- activity in systemic lupus erythematosus patients. Arthritis Rheum. 58, 2481-2487 (2008).
42. Taylor, K. E. et al. Risk alleles for systemic lupus erythematosus in a large case-control collection and associations with clinical subphenotypes. PLoS Genet. 7, e1001311 (2011).
43. Li, Q. Z. et al. The lupus-susceptibility gene kallikrein downmodulates antibody-mediated glomerulonephritis. Genes Immun. 10, 2503-2508 (2009).
44. Scofield, R. H. et al. Klinefelter's syndrome (47,XXY) in male systemic lupus erythematosus patients: support for the notion of a gene-dose effect from the X chromosome. Arthritis Rheum. 58, 2511-2517 (2008).
45. Costenbader, K. H., Feskanich, D., Stampfer, M. J. & Karlson, E. W. Reproductive and menopausal factors and risk of systemic lupus erythematosus in women. Arthritis Rheum. 56, 1251-1262 (2007).
46. Kang, I. et al. Defective control of latent Epstein-Barr virus infection in systemic lupus erythematosus. J. Immunol. 172, 1287-1294 (2004).
47. Yadav, P. et al. Antibodies elicited in response to EBNA-1 may cross-react with dsDNA. PLoS ONE 6, e14488 (2011).
48. Gorelik, G. et al. Impaired T cell protein kinase Cactivation decreases ERK pathway signaling in idiopathic and hydralazine-induced lupus. J. Immunol. 179, 5553-5563 (2007).
49. Du, J. et al. DNA methylation pathways and their crosstalk with histone methylation. Nat. Rev. Mol. Cell Biol. 16, 5519-5532 (2015).
50. Costenbader, K. H. et al. Cigarette smoking and the risk of systemic lupus erythematosus: a meta-analysis. Arthritis Rheum. 50, 849-857 (2004).
51. Finckh, A. et al. Occupational silica and solvent exposures and risk of systemic lupus erythematosus in urban women. Arthritis Rheum. 54, 3648-3654 (2006).
52. Stetson, D. B. Endogenous retroelements and autoimmune disease. Curr. Opin. Immunol. 24, 692-697 (2012).
53. Bennett, L. et al. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J. Exp. Med. 197, 711-723 (2003).
54. Baechler, E. C. et al. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc. Natl Acad. Sci. USA 100, 2610-2615 (2003).
55. Crow, M. K., Kirou, K. A. & Wohlgemuth, J. Microarray analysis of interferon-regulated genes in SLE. Autoimmunity 36, 2481-2490 (2003).
56. Lovgren, T. et al. Induction of interferon- production in plasmacytoid dendritic cells by immune complexes containing nucleic acid released by necrotic or late apoptotic cells and lupus IgG. Arthritis Rheum. 50, 1861-1872 (2004).
57. Kirou, K. A. et al. Activation of the interferon- pathway identifies a subgroup of systemic lupus erythematosus patients with distinct serologic features and active disease. Arthritis Rheum. 52, 1491-1503 (2005).
58. Christensen, S. R. et al. Toll-like receptor 7 and TLR9 dictate autoantibody specificity and have opposing inflammatory and regulatory roles in a murine model of lupus. Immunity 25, 1417-1428 (2006).
59. Barrat, F. J. et al. Nucleic acids of mammalian origin can act as endogenous ligands for Toll-like receptors and may promote systemic lupus erythematosus. J. Exp. Med. 202, 1131-1139 (2005).
60. Oliveira, L. et al. Dysregulation of antiviral helicase pathways in systemic lupus erythematosus. Front. Genet. 5, 418 (2014).
61. Gao, D. et al. Activation of cyclic GMP-AMP synthase by self-DNA causes autoimmune diseases. Proc. Natl Acad. Sci. USA 112, E5699-E5705 (2015).
62. Villanueva, E. et al. Netting neutrophils induce endothelial damage, infiltrate tissues, and expose immunostimulatory molecules in systemic lupus erythematosus. J. Immunol. 187, 538-552 (2011).
63. Crispin, J. C., Kyttaris, V. C., Terhorst, C. & Tsokos, G. C. T cells as therapeutic targets in SLE. Nat. Rev. Rheumatol. 6, 317-325 (2010).
64. Ettinger, R. et al. IL-21 and BAFF/BLyS synergize in stimulating plasma cell differentiation from a unique population of human splenic memory B cells. J. Immunol. 178, 2872-2882 (2007).
65. Koshy, M., Berger, D. & Crow, M. K. Increased expression of CD40 ligand on systemic lupus erythematosus lymphocytes. J. Clin. Invest. 98, 2826-2837 (1996).
66. Nambiar, M. P. et al. Reconstitution of deficient T cell receptor chain restores T cell signaling and augments T cell receptor/CD3-induced interleukin-2 production in patients with systemic lupus erythematosus. Arthritis Rheum. 48, 1948-1955 (2003).
67. Gergely, P. Jr et al. Mitochondrial hyperpolarization and ATP depletion in patients with systemic lupus erythematosus. Arthritis Rheum. 46, 175-190 (2002).
68. Coit, P. et al. Genome-wide DNA methylation study suggests epigenetic accessibility and transcriptional poising of interferon-regulated genes in naive CD4+ T cells from lupus patients. J. Autoimmun. 43, 78-84 (2013).
69. Simpson, N. et al. Expansion of circulating T cells resembling follicular helper T cells is a fixed phenotype that identifies a subset of severe systemic lupus erythematosus. Arthritis Rheum. 62, 234-244 (2010).
70. McKinney, E. F. et al. A CD8+ T cell transcription signature predicts prognosis in autoimmune disease. Nat. Med. 16, 586-591 (2010).
71. Xing, Q. et al. Elevated Th17 cells are accompanied by FoxP3+ Treg cells decrease in patients with lupus nephritis. Rheumatol. Int. 32, 949-958 (2012).
72. Lieberman, L. A. & Tsokos, G. C. The IL-2 defect in systemic lupus erythematosus disease has an expansive effect on host immunity. J. Biomed. Biotechnol. 2010, 740619 (2010).
73. Kil, L. P. et al. Btk levels set the threshold for B-cell activation and negative selection of autoreactive B cells in mice. Blood 119, 3744-3756 (2012).
74. Mackay, M. et al. Selective dysregulation of the FcIIB receptor on memory B cells in SLE. J. Exp. Med. 203, 2157-2164 (2006).
75. Avalos, A. M. et al. Differential cytokine production and bystander activation of autoreactive B cells in response to CpG-A and CpG-B oligonucleotides. J. Immunol. 183, 6262-6268 (2009).
76. Hiepe, F. et al. Long-lived autoreactive plasma cells drive persistent autoimmune inflammation. Nat. Rev. Rheumatol. 7, 170-178 (2011).
77. Jacobi, A. M. et al. HLA-DRhigh/CD27high plasmablasts indicate active disease in patients with systemic lupus erythematosus. Ann. Rheum. Dis. 69, 305-308 (2010).
78. Zhu, H. et al. Autoantigen microarray for high-throughput autoantibody profiling in systemic lupus erythematosus. Genomics Proteomics Bioinformatics 13, 210-218 (2015).
79. Chen, Y. et al. Regulation of dendritic cells and macrophages by an anti-apoptotic cell natural antibody that suppresses TLR responses and inhibits inflammatory arthritis. J. Immunol. 183, 1346-1359 (2009).
80. Liu, S. et al. Ongoing immunoglobulin class switch DNA recombination in lupus B cells: analysis of switch regulatory regions. Autoimmunity 37, 1431-1443 (2004).
81. DeGiorgio, L. A. et al. A subset of lupus anti-DNA antibodies cross-reacts with the NR2 glutamate receptor in systemic lupus erythematosus. Nat. Med. 7, 1189-1193 (2001).
82. Podolska, M. J. et al. Inflammatory etiopathogenesis of systemic lupus erythematosus: an update. J. Inflamm. Res. 8, 1161-1171 (2015).
83. Golbus, J. & McCune, W. J. Lupus nephritis. Classification, prognosis, immunopathogenesis, and treatment. Rheum. Dis. Clin. North Am. 20, 213-242 (1994).
84. Clynes, R., Dumitru, C. & Ravetch, J. V. Uncoupling of immune complex formation and kidney damage in autoimmune glomerulonephritis. Science 279, 1052-1054 (1998).
85. Knight, J. S. & Kaplan, M. J. Lupus neutrophils: 'NET' gain in understanding lupus pathogenesis. Curr. Opin. Rheumatol. 24, 441-450 (2012).
86. Bethunaickan, R. et al. A unique hybrid renal mononuclear phagocyte activation phenotype in murine systemic lupus erythematosus nephritis. J. Immunol. 186, 4994-5003 (2011).
87. Hsieh, C. et al. Predicting outcomes of lupus nephritis with tubulointerstitial inflammation and scarring. Arthritis Care Res. (Hoboken) 63, 5865-5874 (2011).
88. Deng, G. M. & Tsokos, G. C. Pathogenesis and targeted treatment of skin injury in SLE. Nat. Rev. Rheumatol. 11, 663-669 (2015).
89. Kaplan, M. J. Premature vascular damage in systemic lupus erythematosus. Autoimmunity 42, 580-586 (2009).
90. McMahon, M. et al. Dysfunctional proinflammatory high-density lipoproteins confer increased risk of atherosclerosis in women with systemic lupus erythematosus. Arthritis Rheum. 60, 2428-2437 (2009).
91. Lewis, M. J. et al. Improved monitoring of clinical response in systemic lupus erythematosus by longitudinal trend in soluble vascular cell adhesion molecule-1. Arthritis Res. Ther. 18, 5 (2016).
92. Gluhovschi, C. et al. What is the significance of HLA-DR antigen expression in the extraglomerular mesangium in glomerulonephritis Hum. Immunol. 73, 1098-1101 (2012).
93. Achtman, J. C. & Werth, V. P. Pathophysiology of cutaneous lupus erythematosus. Arthritis Res. Ther. 17, 182 (2015).
94. Liao, R. et al. Tacrolimus protects podocytes from injury in lupus nephritis partly by stabilizing the cytoskeleton and inhibiting podocyte apoptosis. PLoS ONE 10, e0132724 (2015).
95. Arnold, W. J. (ed.) American Rheumatism Association Glossary Committee: Dictionary of the Rheumatic Diseases. Vol I: Signs and Symptoms (American College of Rheumatology, 1982).
96. Tan, E. M. et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 25, 1271-1277 (1982).
97. Hochberg, M. C. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 40, 1725 (1997).
98. Petri, M. et al. Derivation and validation of the Systemic Lupus International Collaborating Clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum. 64, 2677-2686 (2012).
99. Aggarwal, R. et al. Distinctions between diagnostic and classification criteria? Arthritis Care Res. (Hoboken) 67, 891-897 (2015).
100. Gladman, D. D., Ibanez, D. & Urowitz, M. B. Systemic Lupus Erythematosus Disease Activity Index 2000. J. Rheumatol. 29, 288-291 (2002).
101. Urowitz, M. B. et al. American College of Rheumatology criteria at inception, and accrual over 5 years in the SLICC inception cohort. J. Rheumatol. 41, 875-880 (2014).
102. Ines, L. et al. Clafissification of systemic lupus erythematosus: Systemic Lupus International Collaborating Clinics Versus American College of Rheumatology Criteria. A comparative study of 2,055 patients from a real-life, international systemic lupus erythematosus cohort. Arthritis Care Res. (Hoboken) 67, 1180-1185 (2015).
103. Amezcua-Guerra, L. M., Higuera-Ortiz, V., Arteaga-Garc, U., Gallegos-Nava, S. & Hbe-Tena, C. Performance of the 2012 Systemic Lupus International Collaborating Clinics and the 1997 American College of Rheumatology classification criteria for systemic lupus erythematosus in a real-life scenario. Arthritis Care Res. (Hoboken) 67, 437-441 (2015).
104. Touma, Z., Gladman, D. D. & Urowitz, M. B. in Dubois Lupus Erythematosus and Related Syndromes (eds Wallace, D. J. & Hahn, B. H.) 563-581 (2013).
105. Abu-Shakra, M. et al. Mortality studies in systemic lupus erythematosus. Results from a single center. II. Predictor variables for mortality. J. Rheumatol. 22, 1265-1270 (1995).
106. Steiman, A. J. et al. Prolonged clinical remission in patients with systemic lupus erythematosus. J. Rheumatol. 41, 1808-1816 (2014).
107. Steiman, A. J. et al. Prolonged serologically active clinically quiescent systemic lupus erythematosus: frequency and outcome. J. Rheumatol. 37, 1822-1827 (2010).
108. Franklyn, K. et al. Definition and initial validation of a Lupus Low Disease Activity State (LLDAS). Ann. Rheum. Dis. http://dx.doi.org/10.1136/ annrheumdis-2015-207726 (2015).
109. Gladman, D. et al. The development and initial validation of the Systemic Lupus International Collaborating Clinics/American College of Rheumatology damage index for systemic lupus erythematosus. Arthritis Rheum. 39, 363-369 (1996).
110. Gladman, D. D. et al. The reliability of the Systemic Lupus International Collaborating Clinics/American College of Rheumatology Damage Index in patients with systemic lupus erythematosus. Arthritis Rheum. 40, 809-813 (1997).
111. Rahman, P. et al. Early damage as measured by the SLICC/ACR damage index is a predictor of mortality in systemic lupus erythematosus. Lupus 10, 93-96 (2001).
112. Bruce, I. N. et al. Factors associated with damage accrual in patients with systemic lupus erythematosus: results from the Systemic Lupus International Collaborating Clinics (SLICC) inception cohort. Ann. Rheum. Dis. 74, 1706-1713 (2015).
113. Gladman, D. D. et al. Recommendations for frequency of visits to monitor systemic lupus erythematosus in asymptomatic patients: data from an observational cohort study. J. Rheumatol. 40, 630-633 (2013).
114. Mosca, L. et al. Effectiveness-based guidelines for the prevention of cardiovascular disease in women - 2011 update: a guideline from the American Heart Association. J. Am. Coll. Cardiol. 57, 1404-1423 (2011).
115. Urowitz, M. B., Ibanez, D. & Gladman, D. D. Atherosclerotic vascular events in a single large lupus cohort: prevalence and risk factors. J. Rheumatol. 34, 70-75 (2007).
116. Tunnicliffe, D. J. et al. Diagnosis, monitoring and treatment of systemic lupus erythematosus: a systematic review of clinical practice guidelines. Arthritis Care Res. (Hoboken) 67, 1440-1453 (2015).
117. Mosca, M. et al. European League Against Rheumatism recommendations for monitoring patients with systemic lupus erythematosus in clinical practice and in observational studies. Ann. Rheum. Dis. 69, 1269-1274 (2010).
118. Bultink, I. E. Osteoporosis and fractures in systemic lupus erythematosus. Arthritis Care Res. (Hoboken) 64, 72-78 (2012).
119. Jeltsch-David, H. & Muller, S. Neuropsychiatric systemic lupus erythematosus: pathogenesis and biomarkers. Nat. Rev. Neurol. 10, 579-596 (2014).
120. Ibanez, D. et al. Optimal frequency of visits for patients with systemic lupus erythematosus to measure disease activity over time. J. Rheumatol. 38, 60-63 (2011).
121. Pego-Reigosa, J. M. et al. Efficacy and safety of nonbiologic immunosuppressants in the treatment of nonrenal systemic lupus erythematosus: a systematic review. Arthritis Care Res. (Hoboken) 65, 1775-1785 (2013).
122. Alarcon, 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).
123. Tsakonas, E. et al. A long-term study of hydroxychloroquine withdrawal on exacerbations in systemic lupus erythematosus. The Canadian Hydroxychloroquine Study Group. Lupus 7, 1180-1185 (1998).
124. Chen, Y.-M. et al. Hydroxychloroquine reduces risk of incident diabetes mellitus in lupus patients in a dose-dependent manner: a population based cohort study. Rheumatology (Oxford) 54, 1244-1249 (2015).
125. 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).
126. Wallace, D. J. et al. Safety profile of belimumab: pooled data from placebo-controlled phase 2 and 3 studies in patients with systemic lupus erythematosus. Lupus 22, 1144-1154 (2013).
127. Petri, M. A. et al. Effects of prasterone on disease activity and symptoms in women with active systemic lupus erythematosus. Arthritis Rheum. 50, 2858-2568 (2004)
128. van Vollenhoven, R. F. & McGuire, J. L. Estrogen, progesterone, and testosterone: can they be used to treat autoimmune diseases Cleve. Clin. J. Med. 61, 2276-2284 (1994).
129. Naafs, B. et al. Thalidomide treatment of subacute cutaneous lupus erythematosus. Br. J. Dermatol. 107, 83-86 (1982).
130. Wolfe, F. et al. Fibromyalgia, systemic lupus erythematosus (SLE), and evaluation of SLE activity. J. Rheumatol. 36, 82-88 (2009).
131. Appenzeller, S., Pallone, A. T., Natalin, R. A. & Costallat, L. T. Prevalence of thyroid dysfunction in systemic lupus erythematosus. J. Clin. Rheumatol. 15, 117-119 (2009).
132. Gladman, D. et al. Accrual of organ damage over time in patients with systemic lupus erythematosus. J. Rheumatol. 30, 1955-1959 (2003).
133. Thamer, M. et al. Prednisone, lupus activity and permanent organ damage. J. Rheumatol. 36, 560-564 (2009).
134. Chambers, S. et al. Damage and mortality in a group of British patients with systemic lupus erythematosus followed up for over 10 years. Rheumatology (Oxford) 48, 673-675 (2009).
135. Fischer-Betz, R. et al. Renal outcome in patients with lupus nephritis using a steroid-free regimen of monthly intravenous cyclophosphamide: a prospective observational study. J. Rheumatol. 39, 2211-2217 (2012).
136. Zeher, M. et al. Efficacy and safety of enteric-coated mycophenolate sodium in combination with two glucocorticoid regimens for the treatment of active lupus nephritis. Lupus 20, 1484-1493 (2011).
137. 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).
138. Tak, M. Treatment of severe lupus nephritis: the new horizon. Nat. Rev. Nephrol. 11, 46-61 (2015).
139. 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).
140. 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).
141. Gunnarsson, I. & Jonsdottir, T. Rituximab treatment in lupus nephritis - where do we stand Lupus 22, 381-389 (2013).
142. 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).
143. van Vollenhoven, R. F. Rituximab - shadow, illusion or light? Autoimmun. Rev. 11, 563-567 (2012).
144. US National Library of Medicine. RING - rituximab for lupus nephritis with remission as a goal (RING). ClinicalTrials.gov https://clinicaltrials.gov/ct2/show/ NCT01673295 (2012).
145. Dooley, M. A. et al. Mycophenolate versus azathioprine as maintenance therapy for lupus nephritis. N. Engl. J. Med. 365, 1886-1895 (2011).
146. 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).
147. Pons-Estel, G. et al. Therapeutic plasma exchange for the management of refractory systemic autoimmune diseases: report of 31 cases and review of the literature. Autoimmun. Rev. 10, 679-684 (2011).
148. Schmeding, A. & Schneider, M. Fatigue, health-related quality of life and other patient-reported outcomes in systemic lupus erythematosus. Best Prac. Res. Clin. Rheumatol. 27, 363-375 (2013).
149. Yelin, E. et al. Work dynamics among persons with systemic lupus erythematosus. Arthritis Rheum. 57, 356-363 (2007).
150. Gordon, C. et al. The substantial burden of systemic lupus erythematosus on the productivity and careers of patients: a European patient-driven online survey. Rheumatology (Oxford) 52, 2292-2301 (2013).
151. Yazdany, J. Health-related quality of life measurement in adult systemic lupus erythematosus: Lupus Quality of Life (LupusQoL), Systemic Lupus Erythematosus-Specific Quality of Life Questionnaire (SLEQOL), and Systemic Lupus Erythematosus Quality of Life Questionnaire (L-QoL). Arthritis Care Res. (Hoboken) 63, S2413-S2419 (2011).
152. Gladman, D. et al. Systemic Lupus International Collaborating Clinics conference on assessment of lupus flare and quality of life measures in SLE. Systemic Lupus International Collaborating Clinics Group. J. Rheumatol 23, 1953-1955 (1996).
153. Dua, A. B. et al. Top 10 recent developments in health-related quality of life in patients with systemic lupus erythematosus. Curr. Rheumatol. Rep. 15, 380 (2013).
154. Ahn, G. E. & Ramsey-Goldman, R. Fatigue in systemic lupus erythematosus. Int. J. Clin. Rheumtol. 7, 217-227 (2012).
155. Ruiz-Irastorza, G., Gordo, S., Olivares, N., Egurbide, M.-V. & Aguirre, C. Changes in vitamin D levels in patients with systemic lupus erythematosus: effects on fatigue, disease activity, and damage. Arthritis Care Res. (Hoboken) 62, 1160-1165 (2010).
156. Furie, R. et al. Clinical, laboratory and health-related quality of life correlates of Systemic Lupus Erythematosus Responder Index response: a post hoc analysis of the phase 3 belimumab trials. Lupus Sci. Med. 1, e000031 (2014).
157. Hanly, J. G. et al. Mood disorders in systemic lupus erythematosus: results from an international, inception cohort study. Arthritis Rheum. 67, 1837-1847 (2015).
158. Ruiz-Arruza, I. et al. Glucocorticoids and irreversible damage in patients with systemic lupus erythematosus. Rheumatology (Oxford) 53, 1470-1476 (2014).
159. Scofield, L., Reinlib, L., Alarco?n, G. S. & Cooper, G. S. Employment and disability issues in systemic lupus erythematosus: a review. Arthritis Care Res. (Hoboken) 59, 1475-1479 (2008).
160. Arbuckle, M. R. et al. Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N. Engl. J. Med. 349, 1526-1533 (2003).
161. James, J. A. et al. Hydroxychloroquine sulfate treatment is associated with later onset of systemic lupus erythematosus. Lupus 16, 1401-1409 (2007).
162. Doria, A. et al. Long-term prognosis and causes of death in systemic lupus erythematosus. Am. J. Med. 119, 700-706 (2006).
163. Abd-Elkareem, M. I., Al Tamimy, H. M., Khamis, O. A., Abdellatif, S. S. & Hussein, M. R. Increased urinary levels of the leukocyte adhesion molecules ICAM-1 and VCAM-1 in human lupus nephritis with advanced renal histological changes: preliminary findings. Clin. Exp. Nephrol. 14, 548-557 (2010).
164. Xuejing, Z. et al. Urinary TWEAK level as a marker of lupus nephritis activity in 46 cases. J. Biomed. Biotechnol. 2012, 359647 (2012).
165. Lapteva, L. et al. Anti-N-methyl-d-aspartate receptor antibodies, cognitive dysfunction, and depression in systemic lupus erythematosus. Arthritis Rheum. 54, 2505-2514 (2006).
166. Kowal, C. et al. Human lupus autoantibodies against NMDA receptors mediate cognitive impairment. Proc. Natl Acad. Sci. USA 103, 19854-19859 (2006).
167. Urowitz, M. B. et al. The bimodal mortality pattern of systemic lupus erythematosus. Am. J. Med. 60, 19221-19225 (1976)
168. Magder, L. S. & Petri, M. Incidence of and risk factors for adverse cardiovascular events among patients with systemic lupus erythematosus. Am. J. Epidemiol. 176, 708-719 (2012).
169. Esdaile, J. M. et al. Traditional Framingham risk factors fail to fully account for accelerated atherosclerosis in systemic lupus erythematosus. Arthritis Rheum. 44, 2331-2337 (2001).
170. Bertsias, G. et al. EULAR recommendations for the management of systemic lupus erythematosus. Report of a Task Force of the EULAR Standing Committee for International Clinical Studies Including Therapeutics. Ann. Rheum. Dis. 67, 195-120 (2008).
171. Lai, C. H. et al. Outcomes of percutaneous coronary intervention in patients with rheumatoid arthritis and systemic lupus erythematosus: an 11-year nationwide cohort study. Ann. Rheum. Dis. http://dx.doi.org/ 10.1136/annrheumdis-2015-207719 (2015).
172. Myasoedova, E. et al. Lipid paradox in rheumatoid arthritis: the impact of serum lipid measures and systemic inflammation on the risk of cardiovascular disease. Ann. Rheum. Dis. 70, 482-487 (2011).
173. 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).
174. Drenkard, C. et al. Remission of systematic lupus erythematosus. Medicine 75, 88-98 (1996).
175. Nossent, J. et al. Disease activity and damage accrual during the early disease course in a multinational inception cohort of patients with systemic lupus erythematosus. Lupus 19, 949-956 (2010).
176. Zen, M. et al. Prolonged remission in Caucasian patients with SLE: prevalence and outcomes. Ann. Rheum. Dis. 74, 2117-2122 (2015).
177. Urowitz, M. B. et al. Prolonged remission in systemic lupus erythematosus. J. Rheumatol 8, 1467-1472 (2005).
178. Mosca, M. et al. Treat-to-target in systemic lupus erythematosus: where are we today? Clin. Exp. Rheum. 30, S112-S115 (2012).
179. US FDA. Guidance for Industry. Systemic Lupus Erythematosus - Developing Medical Products for Treatment (FDA, 2010)
180. Wallace, D. J. et al. Efficacy and safety of epratuzumab in patients with moderate/severe active systemic lupus erythematosus: results from EMBLEM, a phase IIb, randomised, double-blind, placebo-controlled, multicentre study. Ann. Rheum. Dis. 73, 183-190 (2014).
181. Clowse, M. E. B. et al. Efficacy safety epratuzumab patients with moderate-to-severe system. lupus erythematosus: results from two phase 3 randomized, placebo-controlled trials. Arthritis Rheumatol. Abstr. 67 (Suppl. 10), 4L (2015).
182. US National Library of Medicine. Rituximab and belimumab for lupus nephritis. ClinicalTrials.gov https://clinicaltrials.gov/ct2/show/ NCT02260934?term=NCT02260934&rank=1 (2014).
183. Koenen, H. J. et al. A novel bispecific antihuman CD40/CD86 fusion protein with T-cell tolerizing potential. Transplantation 78, 1429-1438 (2004).
184. Kyttaris, V. C., Juang, Y.-T. & Tsokos, G. C. Gene therapy in systemic lupus erythematosus. Lupus 13, 353-358 (2004).
185. Collins, E. & Gilkeson, G. Hematopoetic and mesenchymal stem cell transplantation in the treatment of refractory systemic lupus erythematosus - where are we now? Clin. Immunol. 148, 328-334 (2013).
186. Bombardier, C., Gladman, D. D., Urowitz, M. B., Caron, D. & Chang, C. H. Derivation of the SLEDAI. A disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. Arthritis Rheum. 35, 630-640 (1992).
187. Touma, Z. et al. SLEDAI-2K 10 days versus SLEDAI-2K 30 days in a longitudinal evaluation. Lupus 20, 67-70 (2011).
188. Petri, M. et al. Combined oral contraceptives in women with systemic lupus erythematosus. N. Engl. J. Med. 353, 2550-2558 (2005).
189. Symmons, D. P. et al. Development and assessment of a computerized index of clinical disease activity in systemic lupus erythematosus. Members of the British Isles Lupus Assessment Group (BILAG). Q. J. Med. 69, 927-937 (1988).
190. Isenberg, D. A. et al. BILAG 2004. Development and initial validation of an updated version of the British Isles Lupus Assessment Group's disease activity index for patients with systemic lupus erythematosus. Rheumatology (Oxford) 44, 902-906 (2005).
191. Touma, Z., Gladman, D. D., Ibañez, D. & Urowitz, M.B. Development and initial validation of the Systemic Lupus Erythematosus Disease Activity Index 2000 responder index 50. J. Rheumatol. 38, 275-284 (2011).
192. Furie, R. A. et al. Novel evidence-based systemic lupus erythematosus responder index. Arthritis Rheum. 61, 1143-1151 (2009).
193. Ibanez, D., Gladman, D. D. & Urowitz, M. Summarizing disease features over time: II. Variability measures of SLEDAI-2K. J. Rheumatol. 34, 336-340 (2007).
194. Li, Z.-G., Mu, R., Dai, Z.-P. & Gao, X.-M. T-cell vaccination in systemic lupus erythematosus with autologous activated T-cells. Lupus 14, 884-889 (2005).
195. Ponticelli, C. & Moroni, G. Monoclonal antibodies for systemic lupus erythematosus (SLE). Pharmaceuticals 3, 300-322 (2010).
196. 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).
197. Furie, R. A. et al. A phase 2, randomised, placebo-controlled clinical trial of blisibimod, an inhibitor of B cell activating factor, in patients with moderate-to-severe systemic lupus erythematosus, the PEARL-SC study. Ann. Rheum. Dis. 74, 1667-1675 (2015).
198. Isenberg, D. et al. Efficacy and safety of tabalumab in patients with systemic lupus erythematosus (SLE): results from 2 phase 3, 52-week, multicenter, randomized, placebo-controlled trials. 74, 141 (2015).
199. Alarcon-Segovia, D. et al. LJP 394 for the prevention of renal flare in patients with systemic lupus erythematosus. Arthritis Rheum. 48, 442-454 (2003).
200. Aringer, M. et al. Adverse events and efficacy of anti-TNF- blockade with infliximab in patients with systemic lupus erythematosus: long term follow up of 13 patients. Rheumatology (Oxford) 48, 1451-1454 (2009).
201. Ostendorf, B. et al. Preliminary results of safety and efficacy of the interleukin-1 receptor antagonist anakinra in patients with severe lupus arthritis. Ann. Rheum. Dis. 64, 630-633 (2005).
202. Wallace, D. J. et al. Improvement of disease activity and reduction of severe flares following subcutaneous administration of IL-6 monoclonal antibody (mAb) in subjects with active generalized systemic lupus erythematosus (SLE). ACR http://acrabstracts.org/ abstract/improvement-of-disease-activity-and-reduction-of-severe-flares-following-subcutaneous-administration-of-an-il-6-monoclonal-antibody-mab-in-subjects-with-active-generalized-systemic-lupus-erythematos/ (2014).
203. Llorente, L. et al. Clinical and biologic effects of anti-interleukin-10 monoclonal antibody administration in systemic lupus erythematosus. Arthritis Rheum. 43, 1790-1800 (2000).
204. Khamashta, M. et al. Safety efficacy sifalimumab, anti IFN- monoclonal antibody, phase 2b study moderate severe system. lupus erythematosus (SLE). Arthritis Rheum. Abstr. 66, S312 (2014).
205. Furie, R. et al. Anifrolumab, an anti-interferon receptor monoclonal antibody, in moderate to severe systemic lupus erythematosus (SLE). Arthritis Rheumatol. Abstr. 67 (Suppl. 10), 3223 (2015).
206. Omdal, R. et al. Fatigue in patients with systemic lupus erythematosus: the psychosocial aspects. J. Rheumatol. 30, 283-287 (2003).
207. Ad hoc Committee on Systemic Lupus Erythematosus Response Criteria for Fatigue. Measurement of fatigue in systemic lupus erythematosus: a systematic review. Arthritis Rheum. 57, 1348-1357 (2007).
208. Hanly, J. G., Omisade, A., Su, L., Farewell, V. & Fisk, J. D. ANAM: automated psychological assessment metrics assessment of cognitive function in systemic lupus erythematosus, rheumatoid arthritis, and multiple sclerosis by computerized neuropsychological tests. Arthritis Rheum. 62, 1478-1486 (2010).
209. Panopalis, P. et al. The systemic lupus erythematosus tri-nation study: longitudinal changes in physical and mental well-being. Rheumatology (Oxford) 44, 751-755 (2005).
210. Fortin, P. R. et al. Impact of disease activity and cumulative damage on the health of lupus patients. Lupus 7, 101-107 (1998).
211. Alarcon, G. S. et al. Systemic lupus erythematosus in a multiethnic lupus cohort (LUMINA). XVII. Predictors of self-reported health-related quality of life early in the disease course. Arthritis Rheum. 51, 465-474 (2004).
212. Fernandez, M. et al. Using the Short Form 6D, as an overall measure of health, to predict damage accrual and mortality in patients with systemic lupus erythematosus: XLVII, results from a multiethnic US Cohort. Arthritis Rheum. 57, 986-992 (2007).
213. Bertoli, A. M. et al. Systemic lupus erythematosus in a multiethnic US cohort LUMINA (XLI): factors predictive of self-reported work disability. Ann. Rheum. Dis. 66, 12-17 (2007).
214. Baker, K. & Pope, J. Employment and work disability in systemic lupus erythematosus: a systematic review. Rheumatology (Oxford) 48, 281-284 (2009).
215. Panopalis, P., Petri, M., Manzi, S. & the Tri-Nation Study Group. The Systemic Lupus Erythematosus Tri-Nation Study: cumulative indirect costs. Arthritis Rheum. 57, 64-70 (2007).
216. Clarke, A. E., Urowitz, M. B., Monga, N. & Hanly, J. G. Costs associated with severe and nonsevere systemic lupus erythematosus in Canada. Arthritis Care Res. (Hoboken) 67, 431-436 (2015).