Abstract
We aimed to study the mortality among hospitalized patients with systemic lupus erythematosus (SLE). We performed a retrospective cross-sectional study and identified patients with SLE who were hospitalized at Jordan University Hospital (JUH) between 2002 and 2017.There were 990 admissions among which 283 were SLE patients. The mean age at disease onset was 34 ± 12.5 years and the female to male ratio was 8.4:1. Forty patients died during the 15-year period. In-hospital case fatality was 14% over 15 years. For the deceased patients, the female to male ratio was 3.4:1, mean age at disease onset was 27.8 ± 11.5 years, mean age at death was 35.1 ± 12 years, and mean disease duration was 7.5 ± 6.9 years. Twenty patients had disease duration ≤ 5 years. Infection and SLE-related complication contributed equally to mortality in hospitalized SLE patients (42.5% [CI 27.5%–59%] and 40% [95% CI 25%–56.5%], respectively). Infection related mortality compared to SLE-related mortality was associated with younger age and shorter disease duration (29.5 years versus 38.3 years and 6.4 versus 8.7 years, respectively). CRP was higher in infection related mortality compared to SLE-related mortality (131.4 mg/dl versus 87.6 mg/dl, respectively). Most SLE-related deaths were secondary to pulmonary disease. Renal disease did not contribute directly to mortality. No fatalities were attributed to cardiovascular disease (CVD) or cancer. Infection and active SLE accounted for the majority of deaths at a young age. Significant pulmonary related deaths may indicate a change in trends in SLE mortality, as renal related mortality is expected to decline due to proper management.
Similar content being viewed by others
References
Yurkovich M, Vostretsova K, Chen W, Aviña-Zubieta JA (2014) Overall and cause-specific mortality in patients with systemic lupus erythematosus: a meta-analysis of observational studies. Arthritis Care Res 66(4):608–616. https://doi.org/10.1002/acr.22173
Bernatsky S, Boivin JF, Joseph L, Manzi S, Ginzler E, Gladman D, Urowitz M, Fortin P, Petri M, Barr S (2006) Mortality in systemic lupus erythematosus. Arthritis Rheumatol 54(8):2550–2557
Uramoto KM, Michet CJ Jr, Thumboo J, Sunku J, O'Fallon WM, Gabriel SE (1999) Trends in the incidence and mortality of systemic lupus erythematosus, 1950–1992. Arthritis Rheum 42(1):46–50. https://doi.org/10.1002/1529-0131(199901)42:1%3c46:aid-anr6%3e3.0.co;2-2
Hersh AO, Trupin L, Yazdany J, Panopalis P, Julian L, Katz P, Criswell LA, Yelin E (2010) Childhood-onset disease as a predictor of mortality in an adult cohort of patients with systemic lupus erythematosus. Arthritis Care Res 62(8):1152–1159. https://doi.org/10.1002/acr.20179
Anders H-J, Rovin B (2016) A pathophysiology-based approach to the diagnosis and treatment of lupus nephritis. Kidney Int 90(3):493–501
Mohan C, Putterman C (2015) Genetics and pathogenesis of systemic lupus erythematosus and lupus nephritis. Nat Rev Nephrol 11(6):329–341
Li L, Zuo X, Luo H, Li Y, You Y, Duan L, Zhang W, Zhao H, Li T, Ning W, Xie Y, Liu S, Xie X, Jiang Y, Wu S, Zhu H, Zhou Y (2017) Mortality trend of inpatients with connective tissue diseases: 2005–2014. Zhong nan da xue xue bao Yi xue ban = Journal of Central South University Medical Sciences 42(8):927–933. https://doi.org/10.11817/j.issn.1672-7347.2017.08.009
Wadee S, Tikly M, Hopley M (2007) Causes and predictors of death in South Africans with systemic lupus erythematosus. Rheumatol (Oxf) 46(9):1487–1491. https://doi.org/10.1093/rheumatology/kem180
Fei Y, Shi X, Gan F, Li X, Zhang W, Li M, Hou Y, Zhang X, Zhao Y, Zeng X, Zhang F (2014) Death causes and pathogens analysis of systemic lupus erythematosus during the past 26 years. Clin Rheumatol 33(1):57–63. https://doi.org/10.1007/s10067-013-2383-3
Kim WU, Min JK, Lee SH, Park SH, Cho CS, Kim HY (1999) Causes of death in Korean patients with systemic lupus erythematosus: a single center retrospective study. Clin Exp Rheumatol 17(5):539–545
Teh CL, Ling GR (2013) Causes and predictors of mortality in hospitalized lupus patient in Sarawak General Hospital. Malays Lupus 22(1):106–111. https://doi.org/10.1177/0961203312465780
Cervera R, Khamashta MA, Font J, Sebastiani GD, Gil A, Lavilla P, Mejía JC, Aydintug AO, Chwalinska-Sadowska H, de Ramón E (2003) Morbidity and mortality in systemic lupus erythematosus during a 10-year period: a comparison of early and late manifestations in a cohort of 1,000 patients. Medicine 82(5):299–308
Abu-Shakra M, Urowitz M, Gladman D, Gough J (1995) Mortality studies in systemic lupus erythematosus. Results from a single center. I. Causes of death. J Rheumatol 22(7):1259–1264
Lee Y, Choi S, Ji J, Song G (2016) Overall and cause-specific mortality in systemic lupus erythematosus: an updated meta-analysis. Lupus 25(7):727–734
Alarcón GS, McGwin G Jr, Bastian HM, Roseman J, Lisse J, Fessler BJ, Friedman AW, Reveille JD (2001) Systemic lupus erythematosus in three ethnic groups. VIII. Predictors of early mortality in the LUMINA cohort. Arthritis Care Res 45(2):191–202
Jakes RW, Bae SC, Louthrenoo W, Mok CC, Navarra SV, Kwon N (2012) Systematic review of the epidemiology of systemic lupus erythematosus in the Asia-Pacific region: prevalence, incidence, clinical features, and mortality. Arthritis Care Res 64(2):159–168
Thomas G, Mancini J, Jourde-Chiche N, Sarlon G, Amoura Z, Harlé JR, Jougla E, Chiche L (2014) Mortality associated with systemic lupus erythematosus in France assessed by multiple-cause-of-death analysis. Arthritis Rheumatol 66(9):2503–2511
Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, Schaller JG, Talal N, Winchester RJ (1982) The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 25(11):1271–1277
Sison CP, Glaz J (1995) Simultaneous confidence intervals and sample size determination for multinomial proportions. J Am Stat Assoc 90(429):366–369
Murphy G, Isenberg D (2013) Effect of gender on clinical presentation in systemic lupus erythematosus. Rheumatology 52(12):2108–2115
Jacobsen JP, Ullman S, Junker P, Voss A, Rasmussen JM, Tarp U, Poulsen LH, van Overeem Hansen G, Skaarup B, Hansen TM, Pødenphant J, Halberg PS (1999) Mortality and causes of death of 513 Danish patients with systemic lupus erythematosus. Scand J Rheumatol 28(2):75–80
Heller T, Ahmed M, Siddiqqi A, Wallrauch C, Bahlas S (2007) Systemic lupus erythematosus in Saudi Arabia: morbidity and mortality in a multiethnic population. Lupus 16(11):908–914
Costi LR, Iwamoto HM, Neves DCO, Caldas CAM (2017) Mortality from systemic erythematosus lupus in Brazil: evaluation of causes according to the government health database. Revista brasileira de reumatologia 57(6):574–582. https://doi.org/10.1016/j.rbre.2017.09.001
Voss A, Laustrup H, Hjelmborg J, Junker P (2013) Survival in systemic lupus erythematosus, 1995–2010. A prospective study in a Danish community. Lupus 22(11):1185–1191. https://doi.org/10.1177/0961203313498796
Ward MM, Pyun E, Studenski S (1995) Causes of death in systemic lupus erythematosus. Long-term followup of an inception cohort. Arthritis Rheumatism 38(10):1492–1499
Lerang K, Gilboe IM, Steinar Thelle D, Gran JT (2014) Mortality and years of potential life loss in systemic lupus erythematosus: a population-based cohort study. Lupus 23(14):1546–1552. https://doi.org/10.1177/0961203314551083
Mu L, Hao Y, Fan Y, Huang H, Yang X, Xie A, Zhang X, Ji L, Geng Y, Zhang Z (2018) Mortality and prognostic factors in Chinese patients with systemic lupus erythematosus. Lupus 27(10):1742–1752. https://doi.org/10.1177/0961203318789788
Wu XY, Yang M, Xie YS, Xiao WG, Lin J, Zhou B, Guan X, Luo CN, Che N, Liu XZ, Wang C, Teng JL, Cheng XB, Ye JN, Su YT, Shi H, Yin YF, Liu MR, Sun Y, Hu QY, Zhou ZC, Chi HH, Liu Y, Zhang X, Chen JW, Zhang MJ, Zhao DB, Yang CD, Wu LJ, Liu HL (2018) Causes of death in hospitalized patients with systemic lupus erythematosus: a 10-year multicenter nationwide Chinese cohort. Clin Rheumatol. https://doi.org/10.1007/s10067-018-4259-z
Bosch X, Guilabert A, Pallares L, Cervera R, Ramos-Casals M, Bové A, Ingelmo M, Font J (2006) Infections in systemic lupus erythematosus: a prospective and controlled study of 110 patients. Lupus 15(9):584–589
Gladman D, Hussain F, Iban D, Urowitz M (2002) The nature and outcome of infection in systemic lupus erythematosus. Lupus 11(4):234–239
Zonana-Nacach A, Camargo-Coronel A, Yanez P, Sánchez L, Jimenez-Balderas F, Fraga A (2001) Infections in outpatients with systemic lupus erythematosus: a prospective study. Lupus 10(7):505–510
Goldblatt F, Chambers S, Rahman A, Isenberg DA (2009) Serious infections in British patients with systemic lupus erythematosus: hospitalisations and mortality. Lupus 18(8):682–689. https://doi.org/10.1177/0961203308101019
Feldman CH, Marty FM, Winkelmayer WC, Guan H, Franklin JM, Solomon DH, Costenbader KH, Kim SC (2017) Comparative rates of serious infections among patients with systemic lupus erythematosus receiving immunosuppressive medications. Arthritis Rheumatol 69(2):387–397
Jacobsen S, Petersen J, Ullman S, Junker P, Voss A, Rasmussen JM, Tarp U, Poulsen LH, van Overeem HG, Skaarup B, Hansen TM, Podenphant J, Halberg P (1999) Mortality and causes of death of 513 Danish patients with systemic lupus erythematosus. Scand J Rheumatol 28(2):75–80
Houman M, Smiti-Khanfir M, Ghorbell IB, Miled M (2004) Systemic lupus erythematosus in Tunisia: demographic and clinical analysis of 100 patients. Lupus 13(3):204–211
Al Arfaj A, Khalil N (2009) Clinical and immunological manifestations in 624 SLE patients in Saudi Arabia. Lupus 18(5):465–473
Koh E, Seow A, Leong K, Chng H (1997) SLE mortality in an oriental population. Lupus 6(1):27–31
Fatemi A, Shamsaee S, Raeisi A, Sayedbonakdar Z, Smiley A (2017) Prognostic factors of mortality in Iranian patients with systemic lupus erythematosus admitted to intensive care unit. Clin Rheumatol 36(11):2471–2477. https://doi.org/10.1007/s10067-017-3808-1
Finucci Curi P, Pierrestegui M, Ortiz A, Ceccato F, Paira S (2015) Pulmonary hemorrhage in patients with systemic lupus erythematosus. Clinical manifestations and prognosis. Med Clin (Barc) 145(9):375–379. https://doi.org/10.1016/j.medcli.2014.07.034
Kwok SK, Moon SJ, Ju JH, Park KS, Kim WU, Cho CS, Kim HY, Park SH (2011) Diffuse alveolar hemorrhage in systemic lupus erythematosus: risk factors and clinical outcome: results from affiliated hospitals of Catholic University of Korea. Lupus 20(1):102–107. https://doi.org/10.1177/0961203310381511
Martinez-Martinez MU, Abud-Mendoza C (2011) Predictors of mortality in diffuse alveolar haemorrhage associated with systemic lupus erythematosus. Lupus 20(6):568–574. https://doi.org/10.1177/0961203310392430
Moss KE, Ioannou Y, Sultan SM, Haq I, Isenberg DA (2002) Outcome of a cohort of 300 patients with systemic lupus erythematosus attending a dedicated clinic for over two decades. Ann Rheum Dis 61(5):409–413
Schoenfeld SR, Kasturi S, Costenbader KH (2013) The epidemiology of atherosclerotic cardiovascular disease among patients with SLE: a systematic review. Semin Arthritis Rheum 43(1):77–95. https://doi.org/10.1016/j.semarthrit.2012.12.002
Urowitz MB, Bookman AA, Koehler BE, Gordon DA, Smythe HA, Ogryzlo MA (1976) The bimodal mortality pattern of systemic lupus erythematosus. Am J Med 60(2):221–225
Funding
This work received no funding.
Author information
Authors and Affiliations
Contributions
KM had full access to all the data in the study and takes responsibility for the integrity of data and the accuracy of the data analysis. All authors contributed to the study conception and design. Material preparation and data collection were done by KM, UQ. Data analysis, interpretation, and manuscript writing were performed by KM, MA. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This study was approved by the IRB Committee of Jordan University Hospital (approval number and dates: 2018/62, 30 January 2017).
Informed consent
Informed consent was waived by IRB because the study was considered minimal risk.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Adwan, M.H., Qasem, U. & Mustafa, K.N. In-hospital mortality in patients with systemic lupus erythematosus: a study from Jordan 2002–2017. Rheumatol Int 40, 711–717 (2020). https://doi.org/10.1007/s00296-020-04538-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00296-020-04538-z