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Review

Predicting lupus flares: epidemiological and disease related risk factors

, , & ORCID Icon
Pages 143-153 | Received 19 Sep 2020, Accepted 14 Dec 2020, Published online: 22 Jan 2021

References

  • de Amorim JC, Frittoli RB, Pereira D, et al. Epidemiology, characterization, and diagnosis of neuropsychiatric events in systemic lupus erythematosus. Expert Rev Clin Immunol. 2019;15(4):407–416.
  • Steiman AJ, Urowitz MB, Ibanez D, et al. Prolonged clinical remission in patients with systemic lupus erythematosus. J Rheumatol. 2014;41(9):1808–1816.
  • Morand EF, Mosca M. Treat to target, remission and low disease activity in SLE. Best Pract Res: Clin Rheumatol. 2017;31(3):342–350.
  • Ruperto N, L M H, G S A, et al. International consensus for a definition of disease flare in lupus. Lupus. 2011;20:453–462.
  • Conti F, Ceccarelli F, Perricone C, et al. Flare, persistently active disease, and serologically active clinically quiescent disease in systemic lupus erythematosus: a 2-year follow-up study. PLoS One. 2012;7(9):e45934.
  • Ines L, Duarte C, Silva RS, et al. Identification of clinical predictors of flare in systemic lupus erythematosus patients: a 24-month prospective cohort study. Rheumatology (Oxford). 2014;53(1):85–89.
  • Nikpour M, Urowitz MB, Ibanez D, et al. Frequency and determinants of flare and persistently active disease in systemic lupus erythematosus. Arthritis Rheum. 2009;61(1152–8):64.
  • Petri M, Singh S, Tesfasyone H, et al. Prevalence of flare and influence of demographic and serologic factors on flare risk in systemic lupus erythematosus: a prospective study. J Rheumatol. 2009;36(11):2476–2480.
  • Zen M, Bassi N, Nalotto L, et al. Disease activity patterns in a monocentric cohort of SLE patients: a seven-year follow-up study. Clin Exp Rheumatol. 2012;30:856–863.
  • Illei GG, Takada K, Parkin D, et al. Renal flares are common in patients with severe proliferative lupus nephritis treated with pulse immunosuppressive therapy: long-term follow-up of a cohort of 145 patients participating in randomized controlled studies. Arthritis Rheum. 2002;46:995–1002.
  • Ioannidis JP, Boki KA, Katsorida ME, et al. Remission, relapse, and re-remission of proliferative lupus nephritis treated with cyclophosphamide. Kidney Int. 2000;57:258–264.
  • Moroni G, Quaglini S, Gallelli B, et al. The long-term outcome of 93 patients with proliferative lupus nephritis. Nephrol Dial Transplant. 2007;22(9):2531–2539.
  • Mosca M, Bencivelli W, Neri R, et al. Renal flares in 91 SLE patients with diffuse proliferative glomerulonephritis. Kidney Int. 2002;61(4):1502–1509.
  • Parikh SV, Nagaraja HN, Hebert L, et al. Renal flare as a predictor of incident and progressive CKD in patients with lupus nephritis. Clin J Am Soc Nephrol. 2014;9(2):279–284.
  • Ugarte-Gil MF, Acevedo-Vasquez E, Alarcon GS, et al., The number of flares patients experience impacts on damage accrual in systemic lupus erythematosus: data from a multiethnic Latin American cohort. Ann Rheum Dis. 2015; 74(6): 1019–1023.
  • Zhu TY, Tam LS, Lee VW, et al. Relationship between flare and health- related quality of life in patients with systemic lupus erythematosus. J Rheumatol. 2010;37(3):568–573.
  • Bandeira M, Buratti S, Bartoli M, et al. Relationship between Damage Accrual, Disease Flares And Cumulative Drug Therapies In Juvenile-Onset Systemic Lupus Erythematosus. Lupus. 2006;15(8):515–520.
  • Stoll T, Sutcliffe N, Mach J, et al. Analysis of the relationship between disease activity and damage in patients with systemic lupus erythematosus—a 5-yr prospective study. Rheumatology (Oxford). 2004;43:1039–1044.
  • Zhu TY, Tam LS, Lee VW, et al., The impact of flare on disease costs of patients with systemic lupus erythematosus. Arthritis Rheum. 2009; 61(9): 1159–1167.
  • Petri MA, van Vollenhoven RF, Buyon J, et al. Baseline predictors of systemic lupus erythematosus flares: data from the combined placebo groups in the phase III belimumab trials. Arthritis Rheum. 2013;65(8):2143–2153.
  • Narayanan S, Wilson K, Ogelsby A, et al. Economic burden of systemic lupus erythematosus flares and comorbidities in a commercially insured population in the United States. J Occup Environ Med. 2013;55(11):1262–1270.
  • Pollard C, Hartz S, Leage SL, et al. Elicitation of health state utilities associated with varying severities of flares in systemic lupus erythematosus. Health Qual Life Outcomes. 2015;13(1):66.
  • Gensous N, Marti A, Barnetche T, et al. Predictive biological markers of systemic lupus erythematosus flares: a systematic literature review. Arthritis Res. 2017;19:238.
  • Tseng C-E, Buyon JP, Kim M, et al., The effect of moderate-dose corticosteroids in preventing severe flares in patients with serologically active, but clinically stable, systemic lupus erythematosus: findings of a prospective, randomized, double-blind, placebo-controlled trial. Arthritis Rheum. 2006; 54(11): 3623–3632. .
  • Adamichou C, Bertsias G. Flares in systemic lupus erythematosus: diagnosis, risk factors and preventive strategies. Mediterr J Rheumatol. 2017;28(1):4–12.
  • Jung JY, Suh CH. Infection in systemic lupus erythematosus, similarities, and differences with lupus flare. Korean J Intern Med. 2017;32(3):429–438.
  • Barber MRW, Clarke AE. Systemic lupus erythematosus and risk of infection. Expert Rev Clin Immunol. 2020;16(5):527–538.
  • Beça S, Rodríguez-Pinto I, Alba MA, et al. Development and validation of a risk calculator to differentiate flares from infections in systemic lupus erythematosus patients with fever. Autoimmun Rev. 2015;14(7):586–593.
  • Agmon-Levin N, Mosca M, Petri M, et al. Systemic lupus erythematosus one 624 disease or many? Autoimmun Rev. 2012;11:593–595.
  • da Rosa GP, Ortega MF, Teixeira A, et al. Causes and factors related to hospitalizations in patients with systemic lupus erythematosus: analysis of a 20-year period (1995–2015) from a single referral centre in Catalonia. Lupus. 2019;28(9):1158–1166.
  • Ruiz-Irastorza G, Olivares N, Ruiz-Arruza I, et al. Predictors of major infections in systemic lupus erythematosus. Arthritis Res Ther. 2009;11(4):R109. 49.
  • Kivity S, Agmon-Levin N, Blank M, et al. Infections and autoimmunity–friends or foes? Trends Immunol. 2009;8:409–414.
  • Pimentel-Quiroz VR, Ugarte-Gil MF, Harvey GB, et al. Factors predictive of serious infections over time in systemic lupus erythematosus patients: data from a multi-ethnic, multi-national, Latin American lupus cohort. Lupus. 2019;28(9):1101–1110.
  • Jung JY, Yoon D, Choi Y, et al. Associated clinical factors for serious infections in patients with systemic lupus erythematosus. Sci Rep. 2019;9(1):9704.
  • Í R-F, López-Longo J, Galindo-Izquierdo M, et al. Incidence, associated factors and clinical impact of severe infections in a large, multicentric cohort of patients with systemic lupus erythematosus. Semin Arthritis Rheum. 2017;47(1):38–45.
  • Í R-F, López-Longo FJ, Del Campo V, et al. Bacteremia in systemic lupus erythematosus in patients from a Spanish registry: risk factors, clinical and microbiological characteristics, and outcomes. J Rheumatol. 2020;47(2):234–240.
  • González-Echavarri C, Capdevila O, Espinosa G, et al. Infections in newly diagnosed Spanish patients with systemic lupus erythematosus: data from the RELES cohort. Lupus. 2018;27(14):2253–2261.
  • Chen D, Xie J, Chen H, et al. Infection in Southern Chinese patients with systemic lupus erythematosus: spectrum, drug resistance, outcomes, and risk factors. J Rheumatol. 2016;43(9):1650–1656.
  • Feldman CH, Hiraki LT, Winkelmayer WC, et al. Serious infections among adult medicaid beneficiaries with systemic lupus erythematosus and lupus nephritis. Arthritis Rheumatol. 2015;67(6):1577–1585.
  • Bernatsky S, JF B, Joseph L, et al., An international cohort study of cancer in systemic lupus erythematosus. Arthritis Rheum. 2005; 52(5): 1481–1490.
  • Choi MY, Flood K, Bernatsky S, et al. A review on SLE and malignancy. Best Pract Res Clin Rheumatol. 2017;31(3):373–396.
  • Bernatsky S, Ramsey-Goldman R, Gordon C, et al. Prostate cancer in systemic lupus erythematosus. Int J Cancer. 2011;129(12):2966–2969.
  • Dey D, Kenu E, Isenberg DA. Cancer complicating systemic lupus erythematosus–a dichotomy emerging from a nested case-control study. Lupus. 2013;22(9):919–927.
  • Bernatsky S, Boivin JF, Joseph L, et al. Prevalence of factors influencing cancer risk in women with lupus: social habits, reproductive issues, and obesity. J Rheumatol. 2002;29(12):2551–2554.
  • Bin J, Bernatsky S, Gordon C, et al. Lung cancer in systemic lupus erythematosus. Lung Cancer. 2007;56(3):303–306.
  • Bernatsky S, Ramsey-Goldman R, Petri M, et al. smoking is the most significant modifiable lung cancer risk factor in systemic lupus erythematosus. J Rheumatol. 2018;45(3):393–396.
  • Muñoz C, Isenberg DA. Review of major endocrine abnormalities in patients with systemic lupus erythematosus. Clin Exp Rheumatol. 2019;37:791–796.
  • Luo W, Mao P, Zhang L, et al. Association between systemic lupus erythematosus and thyroid dysfunction: a meta-analysis. Lupus. 2018;27(13):2120–2128.
  • Liu YC, Lin WY, Tsai MC, et al. Systemic lupus erythematosus and thyroid disease - Experience in a single medical center in Taiwan. J Microbiol Immunol Infect. 2019;52(3):480–486.
  • Watad A, Cohen AD, Comaneshter D, et al. Hyperthyroidism association with SLE, lessons from real-life data-A case-control study. Autoimmunity. 2016;49(1):17–20.
  • Choudhry KS, Malik MZ, Buggs-Saxton C. Hypercalcemic crisis due to primary hyperparathyroidism in systemic lupus erythematosus (SLE). Lupus. 2013;22(8):847–850.
  • Liaqat A, Barlas A, Barlas T, et al. Imitating a lupus flare: a case report. Cureus. 2020;12(5):e8327.
  • Arnaud L, Mertz P, Gavand PE, et al. Drug-induced systemic lupus: revisiting the everchanging spectrum of the disease using the WHO pharmacovigilance database. Ann Rheum Dis. 2019;78(4):504–508.
  • Wolfe F, Rasker JJ. The Symptom Intensity Scale, fibromyalgia, and the meaning of fibromyalgia-like symptoms. J Rheumatol. 2006;33(11):2291–2299.
  • Middleton GD, Mcfarlin JE, Lipsky PE. The prevalence and clinical impact of fibromyalgia in systemic lupus erythematosus. Arthritis Rheum. 1994;37(8):1181–1188.
  • Gladman DD, Urowitz MB, Gough J, et al. Fibromyalgia is a major contributor to quality of life in lupus. J Rheumatol. 1997;24(11):2145–2148.
  • Valencia-Flores M, Cardiel MH, Santiago V, Resendiz M, et al. Prevalence and factors associated with fibromyalgia in Mexican patients with systemic lupus erythematosus. Lupus. 2004;13(1):4–10.
  • Friedman AW, Tewi MB, Ahn C, et al. Systemic lupus erythematosus in three ethnic groups: XV. Prevalence and correlates of fibromyalgia. Lupus. 2003;12(4):274–279.
  • Huang FF, Fang R, Nguyen MH, et al. Identifying co-morbid fibromyalgia in patients with systemic lupus erythematosus using the multi-dimensional health assessment questionnaire [published online ahead of print, 2020 Aug 2]. Lupus. 2020;29(11):961203320945379.
  • Pope JE. Measuring flares in systemic lupus erythematosus. Rheumatology (Oxford). 2014;53(12):2134–2135.
  • Nikpour M, Urowitz MB, Ibañez D, et al. Frequency and determinants of flare and persistently active disease in systemic lupus erythematosus. Arthritis Rheum. 2009;61(9):1152–1158.
  • Brunner HI, Mina R, Pilkington C, et al., Preliminary criteria for global flares in childhood-onset systemic lupus erythematosus. Arthritis Care Res (Hoboken). 2011; 63(9): 1213–1223.
  • Mikdashi J, Nived O. Measuring disease activity in adults with systemic lupus erythematosus: the challenges of administrative burden and responsiveness to patient concerns in clinical research. Arthritis Res. 2015;17:183.
  • Romero-Diaz J, Isenberg D, Ramsey-Goldman R. Measures of adult systemic lupus erythematosus: updated version of British Isles Lupus Assessment Group (BILAG 2004), European Consensus Lupus Activity Measurements (ECLAM), Systemic Lupus Activity Measure, Revised (SLAM-R), Systemic Lupus Activity Questionnaire for Population Studies (SLAQ), Systemic Lupus Erythematosus Disease Activity Index 2000 (SLEDAI-2K), and Systemic Lupus International Collaborating Clinics/American College of Rheumatology Damage Index (SDI). Arthritis Care Res (Hoboken). 2011;11:S37–46.
  • Liang MH, Socher SA, Larsen MG, et al. Reliability and validity of six systems for the clinical assessment of disease activity in systemic lupus erythematosus. Arthritis Rheum. 1989;32:1107–1118.
  • Ward MM, Marx AS, Barry NN. Comparison of the validity and sensitivity to change of 5 activity indices in systemic lupus erythematosus. J Rheumatol. 2000;27:664–670.
  • Griffiths B, Mosca M, Gordon C. Assessment of patients with systemic lupus erythematosus and the use of lupus disease activity indices. Best Pract Res Clin Rheumatol. 2005;19(5):685–708.
  • Petri M, M Y K, K C K, et al. Combined oral contraceptives in women with systemic lupus erythematosus. N Engl J Med. 2005;353:2550–2558.
  • 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(12):3918–3930.
  • Chessa E, Piga M, Floris A, et al. Use of physician global assessment (PGA) in systemic lupus erythematosus: a systematic review of its psychometric properties. MedRxiv. 2020; 20064683. 10.1101/2020.04.14.20064683 04,14.
  • Gordon C, Sutcliffe N, Skan J, et al. Definition and treatment of lupus flares measured by the BILAG index. Rheumatology (Oxford). 2003;42:1372–1379.
  • Costenbader K, Hoskin B, Atkinson C, et al. assessing the prevalence and use of validated systemic lupus erythematosus disease activity metrics in real world practice. Ann Rheum Dis. 2019;78:807–808.
  • Zen M, Saccon F, Gatto M, et al. Prevalence and predictors of flare after immunosuppressant discontinuation in patients with systemic lupus erythematosus in remission. Rheumatology. 2020;59(7):1591–1598.
  • Steiman AJ, Gladman DD, Ibanez D, et al. Prolonged serologically active clinically quiescent systemic lupus erythematosus: frequency and outcome. J Rheumatol. 2010;37(9):18227.
  • Zen M, Iaccarino L, Gatto M, et al. Prolonged remission in Caucasian patients with SLE: prevalence and outcomes. Ann Rheum Dis. 2015;74(12):2117–2122.
  • Tsang-A-Sjoe MW, Bultink IE, Heslinga M, et al. Both prolonged remission and Lupus Low Disease Activity State are associated with reduced damage accrual in systemic lupus erythematosus. Rheumatology (Oxford). 2017;56(1):121–128.
  • Mok CC, Ho LY, Tse SM, et al. Prevalence of remission and its effect on damage and quality of life in Chinese patients with systemic lupus erythematosus. Ann Rheum Dis. 2017;76(8):1420–1425.
  • González L, Toloza S, McGwin G, et al. Ethnicity in systemic lupus erythematosus (SLE): its influence on susceptibility and outcomes. Lupus. 2013;22(12):1214–1224.
  • To CH, Yu KL, Mok CC. Performance of complement C3, C4 and anti-dsDNA antibody in predicting disease flare in systemic lupus erythematosus: an analysis of data from 6035 clinical visits [abstract]. Arthritis Rheum. 2011;63(Suppl 10):2295.
  • Stojan G, Petri M. Anti-C1q in systemic lupus erythematosus. Lupus. 2016;25(8):873–877.
  • IE C, PE S, Bootsma H, et al. Changes in antibodies to C1q predict renal relapses in systemic lúpus erythematosus. Am J Kidney Dis. 1995;26:595–601.
  • Matrat A, Veysseyre-Balter C, Trolliet P, et al. Simultaneous detection of anti-C1q and anti-double stranded DNA autoantibodies in lupus nephritis: predictive value for renal flares. Lupus. 2011;20(1):28–34.
  • Meyer OC, Nicaise-Roland P, Cadoudal N, et al. Anti-C1q antibodies antedate patent active glomerulonephritis in patients with systemic lupus erythematosus. Arthritis Res Ther. 2009;11(3):R87.
  • Marto N, Bertolaccini ML, Calabuig E, et al. Anti-C1q antibodies in nephritis: correlation between titres and renal disease activity and positive predictive value in systemic lupus erythematosus. Ann Rheum Dis. 2005;64:444–448.
  • Siegert CE, Daha MR, Tseng CM, et al. Predictive value of IgG autoantibodies against C1q for nephritis in systemic lupus erythematosus. Ann Rheum Dis. 1993;52:851–856.
  • Akhter E, Burlingame RW, Seaman AL, et al. Anti-C1q antibodies have higher correlation with flares of lupus nephritis than other serum markers. Lupus. 2011;20(12):1267–1274.
  • Fatemi A, Samadi G, Sayedbonakdar Z, et al. Anti-C1q antibody in patients with lupus nephritic flare: 18-month follow-up and a nested case-control study. Mod Rheumatol. 2016;26(2):233–239.
  • Metwally IM, Eesa NN, Yacoub MH, et al. Association of anti-nucleosome and anti C1q antibodies with lupus nephritis in an Egyptian cohort of patients with systemic lupus erythematosus. Adv Rheumatol. 2019;59(10).
  • Mirzayan MJ, Schmidt RE, Witte T. Prognostic parameters for flare in systemic lupus erythematosus. Rheumatol Oxf Engl. 2000;39:1316–1319.
  • Viallard JF, Bloch-Michel C, Neau-Cransac M, et al. HLA-DR expression on lymphocyte subsets as a marker of disease activity in patients with systemic lupus erythematosus. Clin Exp Immunol. 2001;125(3):485–491.
  • Stojan G, Fang H, Magder L, et al. Erythrocyte sedimentation rate is a predictor of renal and overall SLE disease activity. Lupus. 2013;22(8):827–834.
  • Stojan G, Kvit A, Curriero FC, et al. Analysis of organspecific lupus flares in relation to atmospheric variables and fine particulate matter pollution. Arthritis Rheumatol. 2020;72(7):1134–1142.
  • Richardson RB. Epigenetically altered t cells contribute to lupus flares. Cells. 2019;8(2):127.
  • Costedoat-Chalumeau N, Pouchot J, Guettrot-Imbert G, et al. Adherence to treatment in systemic lupus erythematosus patients. Best Pract Res Clin Rheumatol. 2013;27(3):329–340.
  • Costedoat-Chalumeau N, Galicier L, Aumaître O, et al. Hydroxychloroquine in systemic lupus erythematosus: results of a French multicentre controlled trial (PLUS Study). Ann Rheum Dis. 2013;72(11):1786–1792.
  • Costedoat-Chalumeau N, Houssiau F, Izmirly P, et al. A prospective international study on adherence to treatment in 305 patients with flaring sle: assessment by drug levels and self-administered questionnaires. Clin Pharmacol Ther. 2019 Aug;106(2):374–382.
  • Costedoat-Chalumeau N, Amoura Z, Hulot JS, et al. Low blood concentration of hydroxychloroquine is a marker for and predictor of disease exacerbations in patients with systemic lupus erythematosus. Arthritis Rheum. 2006;54:328490.
  • Cunha C, Alexander S, Ashby D, et al. Hydroxycloroquine blood concentration in lupus nephritis: a determinant of disease outcome? Nephrol Dial Transplant. 2018;33(9):160410.
  • 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(6):958–967.
  • van Vollenhoven R, Voskuyl A, Bertsias G, et al., A framework for remission in SLE: consensus findings from a large international task force on definitions of remission in SLE (DORIS). Ann Rheum Dis. 2017; 76(3): 554–561.
  • Franklyn K, Lau CS, Navarra SV, et al., Definition and initial validation of a lupus low disease activity state (LLDAS). Ann Rheum Dis. 2016; 75(9): 1615–1621.
  • Chen HL, Shen LJ, Hsu PN, et al. Cumulative burden of glucocorticoid-related adverse events in patients with systemic lupus erythematosus: findings from a 12-year longitudinal study. J Rheumatol. 2018;45(1):83–89.
  • Singh JA, Hossain A, Kotb A, et al. Risk of serious infections with immunosuppressive drugs and glucocorticoids for lupus nephritis: a systematic review and network meta-analysis. BMC Med. 2016;14(1):137.
  • Ruiz-Arruza I, Ugarte A, Cabezas-Rodriguez I, et al. Glucocorticoids and irreversible damage in patients with systemic lupus erythematosus. Rheumatology. 2014;53:1470–1476.
  • Al Sawah S, Zhang X, Zhu B, et al. 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. 2015; 21: e000066. Published 2015Mar11
  • Houssiau FA, Vasconcelos C, D’Cruz D, 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. 2002;46(8):2121–2131.
  • Zeher M, Doria A, Lan J, et al. Efficacy and safety of enteric-coated mycophenolate sodium in combination with two glucocorticoid regimens for the treatment of active lupus nephritis. Lupus. 2011;20(14):1484–1493.
  • Ruiz-Arruza I, Lozano J, Cabezas-Rodriguez I, et al. Restrictive use of oral glucocorticoids in systemic lupus erythematosus and prevention of damage without worsening long-term disease control: an observational study. Arthritis Care Res (Hoboken). 2018;70(4):582–591.
  • Fanouriakis A, Bertsias G. Changing paradigms in the treatment of systemic lupus erythematosus. Lupus Sci Med. 2019;6(1):e000310.
  • Ngamjanyaporn P, EM M, JC S, et al. Clinicians approaches to management of background treatment in patients with SLE in clinical remission: results of an international observational survey. Lupus Sci Med. 2017 2017Jun29; 4(1):e000173. Published
  • 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(6):736–745. 2019
  • Tani C, Elefante E, Signorini V, et al. Glucocorticoid withdrawal in systemic lupus erythematosus: are remission and low disease activity reliable starting points for stopping treatment? A real-life experience. RMD Open. 2019;5(2):e000916.
  • Goswami RP, Sit H, Ghosh P, et al. Steroid-free remission in lupus: myth or reality; an observational study from a tertiary referral centre. Clin Rheumatol. 2019;38(4):1089–1097.
  • Mathian A, Pha M, Haroche J, et al. Withdrawal of low-dose prednisone in SLE patients with a clinically quiescent disease for more than 1 year: a randomised clinical trial. Ann Rheum Dis. 2020;79(3):339–346.
  • Strehl C, Bijlsma JW, de Wit M, et al. Defining conditions where long-term glucocorticoid treatment has an acceptably low level of harm to facilitate implementation of existing recommendations: viewpoints from an EULAR task force. Ann Rheum Dis. 2016;75(6):952–957.
  • Aouhab Z, Hong H, Felicelli C, et al. Outcomes of Systemic Lupus Erythematosus in Patients who Discontinue Hydroxychloroquine. ACR Open Rheumatol. 2019;1(9):593–599.
  • Canadian Hydroxychloroquine Study Group. A randomized study of the effect of withdrawing hydroxychloroquine sulfate in systemic lupus erythematosus. N Engl J Med. 1991;324(3):150–154.
  • Pons-Estel GJ. Alarco´ n GS, Hachuel L et al. Rheumatology. 2012;51:129–138.
  • Ugarte-Gil MF, Wojdyla D, Pastor-Asurza CA, et al. Predictive factors of flares in systemic lupus erythematosus patients: data from a multiethnic Latin American cohort. Lupus. 2018;27(4):536–544.
  • Eudy AM, Siega-Riz AM, Engel SM, et al. Effect of pregnancy on disease flares in patients with systemic lupus erythematosus. Ann Rheum Dis. 2018;77:855–860.
  • Jara LJ, Medina G, Cruz-Dominguez P, et al. Risk factors of systemic lupus erythematosus flares during pregnancy. Immunol Res. 2014;60(2–3):184–192.
  • Stojan G, Baer AN. Flares of systemic lupus erythematosus during pregnancy and the puerperium: prevention, diagnosis and management. Expert Rev Clin Immunol. 2012;8(5):439–453.
  • Andreoli L, Bertsias GK, Agmon-Levin N, et al. EULAR recommendations for women’s health and the management of family planning, assisted reproduction, pregnancy and menopause in patients with systemic lupus erythematosus and/or antiphospholipid syndrome. Ann Rheum Dis. 2017;76(3):476–485.
  • Holcombe RF, Baethge BA, Wolf RE, et al. Correlation of serum interleukin-8 and cell surface lysosome-associated membrane protein expression with clinical disease activity in systemic lupus erythematosus. Lupus. 1994;3(2):97–102.
  • Wong CK, Li EK, Ho CY, et al. Elevation of plasma interleukin-18 concentration is correlated with disease activity in systemic lupus erythematosus. Rheumatology (Oxford). 2000;39(10):1078–1081.
  • Ruchakorn N, Ngamjanyaporn P, Suangtamai T, et al. Performance of cytokine models in predicting SLE activity. Arthritis Res Ther. 2019;21:287.
  • Torell F, Eketjäll S, Idborg H, et al. Cytokine Profiles in Autoantibody Defined Subgroups of Systemic Lupus Erythematosus. J Proteome Res. 2019;18(3):1208–1217.
  • Baechler EC, Batliwalla FM, Karypis G, et al. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc Natl Acad Sci U S A. 2003;100(5):2610–2615.
  • Bauer JW, Petri M, Batliwalla FM, et al. Interferon-regulated chemokines as biomarkers of systemic lupus erythematosus disease activity: a validation study. Arthritis Rheum. 2009;60(10):3098–3107.
  • Rose T, Grützkau A, Klotsche J, et al. Are interferon-related biomarkers advantageous for monitoring disease activity in systemic lupus erythematosus? A longitudinal benchmark study. Rheumatology (Oxford). 2017;56(9):1618–1626.
  • Mathian A, Mouries-Martin S, Dorgham K, et al. Monitoring disease activity in systemic lupus erythematosus with single-molecule array digital enzyme-linked immunosorbent assay quantification of serum interferon-α. Arthritis Rheumatol. 2019;71(5):756–765.
  • Petri MA, van Vollenhoven RF, Buyon J, et al. Baseline predictors of systemic lupus erythematosus flares: data from the combined placebo groups in the phase III belimumab trials. Arthritis Rheum. 2013;65(8):2143–2153.
  • Becker-Merok A, Nikolaisen C, Nossent HC. B-lymphocyte activating factor in systemic lupus erythematosus and rheumatoid arthritis in relation to autoantibody levels, disease measures and time. Lupus. 2006;15(9):570–576.
  • Munroe ME, Vista ES, Guthridge JM, et al. Proinflammatory adaptive cytokine and shed tumor necrosis factor receptor levels are elevated preceding systemic lupus erythematosus disease flare. Arthritis Rheumatol. 2014;66(7):1888–1899.
  • Michaelson JS, Wisniacki N, Burkly LC, et al. Role of TWEAK in lupus nephritis: a bench-to-bedside review. J Autoimmun. 2012;39(3):130–142.
  • Panousis NI, Bertsias GK, Ongen H, et al. Combined genetic and transcriptome analysis of patients with SLE: distinct, targetable signatures for susceptibility and severity. Ann Rheum Dis. 2019;78(8):1079–1089.
  • Mackay M, Oswald M, Sanchez-Guerrero J, et al. Molecular signatures in systemic lupus erythematosus: distinction between disease flare and infection. Lupus Sci Med. 2016 Nov 10;3(1):e000159.
  • Lu R, Guthridge JM, Chen H, et al. Immunologic findings precede rapid lupus flare after transient steroid therapy. Sci Rep. 2019 Jun 13;9(1):8590.
  • DD G, MB U, EC K. Serologically active clinically quiescent systemic lupus erythematosus: a discordance between clinical and serologic features. Am J Med. 1979;66(2):210–215.
  • Steiman AJ, Gladman DD, Ibañez D, et al. Prolonged serologically active clinically quiescent systemic lupus erythematosus: frequency and outcome. J Rheumatol. 2010;37(9):1822–1827.
  • Steiman AJ, Gladman DD, Ibañez D, et al. Lack of interferon and proinflammatory cyto/chemokines in serologically active clinically quiescent systemic lupus erythematosus. J Rheumatol. 2015;42(12):2318–2326.
  • Katz P, Nelson WW, Daly RP, et al. PatientReported lupus flare symptoms are associated with worsened patient outcomes and increased economic burden. J Manag Care Spec Pharm. 2020;26(3):275–283.
  • Abu Bakar F, Sazliyana Shaharir S, Mohd R, et al. Burden of systemic lupus erythematosus on work productivity and daily living activity: a cross-sectional study among malaysian multi-ethnic cohort. Arch Rheumatol. 2020;35(2):205–213.
  • Elera-Fitzcarrald C, Fuentes A, González LA, et al. F. Expert Rev Clin Immunol. 2018;14(11):915–931.
  • Katz P, Wan GJ, Daly P, et al. Patient-reported flare frequency is associated with diminished quality of life and family role functioning in systemic lupus erythematosus. Qual Life Res. 2020;29(12):3251–3261.
  • Mok CC, Ho LY, Cheung MY, et al. Effect of disease activity and damage on quality of life in patients with systemic lupus erythematosus: a 2-year prospective study. Scand J Rheumatol. 2009;38(2):121–127.
  • Louthrenoo W, Kasitanon N, Morand E, et al. Comparison of performance of specific (SLEQOL) and generic (SF36) health-related quality of life questionnaires and their associations with disease status of systemic lupus erythematosus: a longitudinal study. Arthritis Res Ther. 2020;22(1):8.
  • Golder V, Kandane-Rathnayake R, Hoi AY, et al. Association of the lupus low disease activity state (LLDAS) with health-related quality of life in a multinational prospective study. Arthritis Res Ther. 2017;19(1):62.
  • Bandeira M, Buratti S, Bartoli M, et al. Relationship between damage accrual, disease flares and cumulative drug therapies in juvenile-onset systemic lupus erythematosus. Lupus. 2006;15(8):515–520.
  • Ceccarelli F, Perricone C, Massaro L, et al. Assessment of disease activity in systemic lupus erythematosus: lights and shadows. Autoimmun Rev. 2015;14(7):601–608.
  • Nossent J, Kiss E, Rozman B, et al. Disease activity and damage accrual during the early disease course in a multinational inception cohort of patients with systemic lupus erythematosus. Lupus. 2010;19(8):949–956.
  • Nossent JC, Cikes N, Kiss E, et al. Current causes of death in systemic lupus erythematosus in Europe, 2000-2004: relation to disease activity and damage accrual. Lupus. 2007;16(5):309–317.
  • Tselios K, Gladman DD, Touma Z, et al. Clinical remission and low disease activity outcomes over 10 years in systemic lupus erythematosus. Arthritis Care Res (Hoboken). 2019;71(6):822–828.

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