Organ damage accrual and distribution in systemic lupus erythematosus patients followed-up for more than 10 years

Abstract

Objective

The aim of this study was to determine the prevalence, predictors and progression of organ damage in a monocentric cohort of systemic lupus erythematosus patients with a long follow-up. Organ damage was assessed by the Systemic Lupus International Collaborating Clinics Damage Index one year after diagnosis and every five years. Disease activity was measured by the systemic lupus erythematosus disease activity index (SLEDAI)-2K at the beginning of the follow-up. Univariate and multivariable analyses were used to detect items associated with damage. A total of 511 systemic lupus erythematosus patients (92% females, 95% Caucasian), prospectively followed from 1972 to 2014, were included.

Results

After a mean disease duration of 16 years (SD: 9.5) and a mean follow-up of 12.9 years (SD: 8.8), 354 patients (69.3%) had accrued some damage: 49.7% developed mild/moderate damage, while 19.5% showed severe damage. Damage was evident in 40% of 511 patients one year after diagnosis, and its prevalence linearly increased over time. Longer disease duration, higher SLEDAI, severe Raynaud’s, chronic alopecia and cerebral ischaemia were significantly associated with organ damage. No associations between damage and autoantibodies, including anti-dsDNA, anti-Sm or antiphospholipid antibodies, were observed. Anyway, antiphospholipid syndrome and anticardiolipin antibodies predicted the development of neuropsychiatric damage. The ocular, musculoskeletal and neuropsychiatric systems were the most frequently damaged organs, with a linear increase during follow-up.

Conclusion

A high rate of moderate and severe damage has been detected early in a wide cohort of young lupus patients, with a linear trend of increase over time. Disease activity and long duration of disease predict damage, while antiphospholipid antibodies play a role in determining neuropsychiatric damage.

Keywords

Systemic lupus erythematosus damage disease activity antiphospholipid antibodies neuropsychiatric damage

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References

Urowitz

Gladman

Tom

et al.

Changing patterns in mortality and disease outcomes for patients with systemic lupus erythematosus. J Rheumatol 2008; 35: 2152–2158.

Urowitz

Bookman

Koehfler

et al.

The bimodal mortality pattern of systemic lupus erythematosus. Am J Med 1976; 60: 221–225.

Sutton

Davidson

Bruce

. The Systemic Lupus International Collaborating Clinics (SLICC) Damage Index: A systemic literature review. Semin Arthritis Rheum 2013; 43: 352–361.

Gladman

Ginzler

Goldsmith

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 1996; 39: 363–369.

Fredi

Cavazzana

Taraborelli

et al.

Prolonged assumption of HCQ is associated with longer survival in SLE. Ann Rheum Dis 2014; 73: 77–77.

Ruiz-Irastorza

Egurbide

Ugalde

et al.

High Impact of Antiphospholipid Syndrome on Irreversible Organ Damage and Survival of Patients with Systemic Lupus Erythematosus. Arch Intern Med 2004; 164: 77–82.

Taraborelli

Leuenberger

Lazzaroni

et al.

The contribution of antiphospholipid antibodies to organ damage in systemic lupus erythematosus. Lupus 2016; 25: 1365–1368.

Petri

Purvey

Fang

Magder

. Predictors of organ damage in systemic lupus erythematosus: the Hopkins Lupus Cohort. Arthritis Rheum 2012; 64: 4021–4028.

Ruiz-Irastorza

Egurbide

Martinez-Berriotxoa

et al.

Antiphospholipid antibodies predict damage in patients with systemic lupus erythematosus. Lupus 2004; 13: 900–905.

10.

Conti

Ceccarelli

Perricone

et al.

The chronic damage in systemic lupus erythematosus is driven by flares, glucocorticoids and antiphospholipid antibodies: results from a monocentric cohort. Lupus 2016; 25: 719–726.

11.

Hochberg

. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1997; 40: 1725–1725.

12.

Gladman

Ibanez

Urowitz

. Systemic lupus erythematosus disease activity index 2000. J Rheumatol 2002; 29: 288–291.

13.

Bernstein

Bunn

Hughes

GRV

. Identification of antibodies to acidic antigens by counterimmunoelectrophoresis. Ann Rheum Dis 1982; 41: 554–555.

14.

Harris

. The Second International anti-cardiolipin standardization workshop. The Kingston anti-phospholipid antibody study (KAPS) group. Ann J Clin Pathol 1990; 94: 476–484.

15.

Balestrieri

Tincani

Spatola

et al.

Anti-ß2 glycoprotein I: a marker of antiphospholipid syndrome?

Lupus 1995; 4: 122–130.

16.

Gladman

Urowitz

Rahman

Ibanez

Tam

. Accrual of organ damage over time in patients with systemic lupus erythematosus. J Rheumatol 2003; 30: 1955–1959.

17.

Chambers

Allen

Rahman

Isenberg

. Damage and mortality in a group of British patients with systemic lupus erythematosus followed up for over 10 years. Rheumatology (Oxford) 2009; 48: 673–675.

18.

Estevez del Toro

Chico Capote

Hechavarria

et al.

Damage in cuban patients with systemic lupus erythematosus. Relation with disease features. Rheumatol Clin 2010; 6: 11–15.

19.

Becker-Merok

Nossent

. Damage accumulation in systemic lupus erythematosus and its relation to disease activity and mortality. J Rheumatol 2006; 33: 1570–1577.

20.

Nossent

Kiss

Rozman

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: 949–956.

21.

Al Sawah

Zhang

Zhu

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; 2: e000066–e000066.

22.

Bruce

O’Kneeffe

Farewell

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 2015; 74: 1706–1713.

23.

Stoll

Sutcliff

Mach

Klaghofer

Isenberg

. 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.

24.

Lopez

Davidson

Beeby

Egger

Isenberg

. Lupus disease activity and risk of subsequent organ damage and mortality in a large lupus cohort. Rheumatology (Oxford) 2012; 51: 491–498.

25.

Nossent

. SLICC/ACR damage Index in Afro-Carribean patients with systemic lupus erythematosus: changes in and relationship to disease activity, corticosteroid therapy, and prognosis. J Rheumatol 1998; 25: 654–659.

26.

Santos

Vinagre

Nero

et al.

Predictors of damage progression in Portuguese patients with Systemic Lupus Erythematosus. Cont Challages Rheumatol. Ann NY Acad Sci 2009; 1173: 822–828.

27.

Stoll

Seifert

Isenberg

. SLICC/ACR Damage index is valid, and renal ad pulmonary orgen scores are predictors of severe outcome in patients with systemic lupus erythematosus. Lupus 2004; 13: 900–905.

28.

Alarcon

Roseman

McGwin

Jr et al.

Systemic lupus erythematosus in three ethnic groups. XX. Damage as a predictor of further damage. Rheumatology (Oxford) 2004; 43: 202–205.

29.

Zonana-Nacach

Camargo-Coronel

Yanez

et al.

Measurement of damage in 210 Mexican patients with systemic lupus erythematosus: relationship with disease duration. Lupus 1998; 7: 119–123.

30.

Sung

Hur

Sinskey

et al.

Assessment of damage in Korean patients with systemic lupus erythematosus. J Rheumatol 2007; 34: 987–991.

31.

Swaak

Groenwold

Brosveld

. Predictive value of complement profile and anti-dsDNA in systemic lupus erythematosus. Ann Rheum Dis 1986; 45: 359–366.

32.

ter Borg

Horst

Hummel

Limburg

Kallenberg

. Measurement of increases in anti-double-stranded DNA antibody levels as a predictor of disease exacerbation in systemic lupus erythematosus. Arthritis Rheum 1990; 33: 634–643.

33.

Yee

Hussein

Skan

Bowman

Situnayake

Gordon

. Association of damage with autoantibody profile, age, race, sex and disease duration in systemic lupus erythematosus. Rheumatology 2003; 42: 276–279.

34.

Govoni

Bombardieri

Bortoluzzi

et al.

Factors and comorbidities associated with first neuropsychiatric event in systemic lupus erythematosus: does a risk profile exist? A large multicentre retrospective cross-sectional study on 959 Italian patients. Rheumatology (Oxford) 2012; 51: 157–168.

35.

Muscal

Brey

. Antiphospholipid syndrome and the brain in pediatric and adult patients. Lupus 2010; 19: 406–411.

36.

Bonakdar

Mohtashmam

Karimifar

. Evaluation of damage index and its association with risk factor in patients with systemic lupus erythematosus. J Res Med Sci 2011; 16: S427–S432.

37.

Zonana-Nacach

Barr

Magder

Petri

. Damage in systemic lupus erythematosus and its association with corticosteroids. Arthritis Rheum 2000; 43: 1801–1808.

38.

Alderaan

Sekiki

Magder

Petri

. Risk factors for cataracts in systemic lupus erythematosus (SLE). Rheumatol Int 2015; 35: 701–708.

39.

Petri

. Musculo-skeletal complications of systemic lupus erythematosus in the Hopkins Lupus Cohort: an update. Arthritis Care Res 1995; 8: 137–145.