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Causes of death in hospitalized patients with systemic lupus erythematosus: a 10-year multicenter nationwide Chinese cohort

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Abstract

To estimate the mortality and describe the causes of death in a large multicenter cohort of hospitalized patients with SLE in China. This was a retrospective study of a nationwide SLE cohort (10 centers, 29,510 hospitalized patients) from 2005 to 2014 in China. Standardized mortality ratios (SMRs) were calculated for all death and were stratified by sex and age. Chi-square test was used to determine whether the major causes of death vary in age, sex, duration of SLE, disease activity, or medications. Comparison between dead patients and survival controls was used to identify the risk factors for mortality. Logistic regression analysis was used to evaluate the risk factors for mortality. A total of 360 patients died during the study period, accounting for 1.22%. The overall SMR was 2.13 (95% CI 1.96, 2.30), with a particularly high SMR seen in subgroups characterized by younger age. Infection (65.8%) was the most common cause of death, followed by lupus nephritis (48.6%), hematological abnormality (18.1%), neuropsychiatric lupus/NPSLE (15.8%), and interstitial pneumonia (13.1%). Cardiovascular disease and malignancy contributed little to the causes of death. Infection, in particular severe pulmonary infection, emerged as the foremost risk factor for mortality, followed by lupus encephalopathy. However, lupus nephritis and hematological abnormalities occurred more frequently in survival patients. SLE patients at a younger age of diagnosis have a poorer prognosis. Infection dominated the causes of death in recent China. Ethnicity and medications might account for the differences in causes of death compared with western populations.

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References

  1. Borchers AT, Keen CL, Shoenfeld Y, Gershwin ME (2004) Surviving the butterfly and the wolf: mortality trends in systemic lupus erythematosus. Autoimmun Rev 3:423–453

    Article  PubMed  Google Scholar 

  2. Henderson L, Masson P, Craig JC, Flanc RS, Roberts MA, Strippoli GF et al (2012) Treatment for lupus nephritis. The Cochrane database of systematic reviews, p CD002922

  3. 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 42:46–50

    Article  CAS  PubMed  Google Scholar 

  4. Wang Z, Wang Y, Zhu R, Tian X, Xu D, Wang Q et al (2015) Long-term survival and death causes of systemic lupus erythematosus in China: a systemic review of observational studies. Medicine:e794

  5. Alamanos Y, Voulgari PV, Papassava M, Tsamandouraki K, Drosos AA (2003) Survival and mortality rates of systemic lupus erythematosus patients in northwest Greece. Study of a 21-year incidence cohort. Rheumatology:1122–1123

  6. Doria A, Iaccarino L, Ghirardello A, Zampieri S, Arienti S, Sarzi-Puttini P, Atzeni F, Piccoli A, Todesco S (2006) Long-term prognosis and causes of death in systemic lupus erythematosus. Am J Med 119:700–706

    Article  PubMed  Google Scholar 

  7. 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:1546–1552

  8. Fors Nieves CE, Izmirly PM (2016) Mortality in systemic lupus erythematosus: an updated review. Curr Rheumatol Rep:21

  9. Bernatsky S, Boivin JF, Joseph L, Manzi S, Ginzler E, Gladman DD, Urowitz M, Fortin PR, Petri M, Barr S, Gordon C, Bae SC, Isenberg D, Zoma A, Aranow C, Dooley MA, Nived O, Sturfelt G, Steinsson K, Alarcón G, Senécal JL, Zummer M, Hanly J, Ensworth S, Pope J, Edworthy S, Rahman A, Sibley J, el-Gabalawy H, McCarthy T, St. Pierre Y, Clarke A, Ramsey-Goldman R (2006) Mortality in systemic lupus erythematosus. Arthritis Rheum 54:2550–2557

    Article  CAS  PubMed  Google Scholar 

  10. Yurkovich M, Vostretsova K, Chen W, Avina-Zubieta JA (2014) Overall and cause-specific mortality in patients with systemic lupus erythematosus: a meta-analysis of observational studies. Arthritis Care Res 66:608–616

    Article  Google Scholar 

  11. Dubois EL, Wierzchowiecki M, Cox MB, Weiner JM (1974) Duration and death in systemic lupus erythematosus. An analysis of 249 cases. Jama:1399–1402

  12. Wallace DJ, Podell T, Weiner J, Klinenberg JR, Forouzesh S, Dubois EL (1981) Systemic lupus erythematosus--survival patterns. Experience with 609 patients. Jama:934–938

  13. Rees F, Doherty M, Grainge MJ, Lanyon P, Davenport G, Zhang W (2016) Mortality in systemic lupus erythematosus in the United Kingdom 1999-2012. Rheumatology:854–860

  14. Urowitz MB, Bookman AA, Koehler BE, Gordon DA, Smythe HA, Ogryzlo MA (1976) The bimodal mortality pattern of systemic lupus erythematosus. Am J Med 60:221–225

    Article  CAS  PubMed  Google Scholar 

  15. Reveille JD, Bartolucci A, Alarcon GS (1990) Prognosis in systemic lupus erythematosus. Negative impact of increasing age at onset, black race, and thrombocytopenia, as well as causes of death. Arthritis Rheum:37–48

  16. Ward MM, Pyun E, Studenski S (1995) Causes of death in systemic lupus erythematosus. Long-term followup of an inception cohort. Arthritis Rheum 38:1492–1499

    Article  CAS  PubMed  Google Scholar 

  17. Cervera R, Khamashta MA, Font J, Sebastiani GD, Gil A, Lavilla P et al (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:299–308

  18. 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:409–413

  19. Mok CC, Mak A, Chu WP, Toa CH, Wong SN (2005) Long-term survival of southern Chinese patients with systemic lupus erythematosus: a prospective study of all age-groups. Medicine:218–224

  20. Wu G, Jia X, Gao D, Zhao Z (2014) Survival rates and risk factors for mortality in systemic lupus erythematosus patients in a Chinese center. Clin Rheumatol 33:947–953

    Article  PubMed  Google Scholar 

  21. Feng X, Zou Y, Pan W, Wang X, Wu M, Zhang M et al (2011) Prognostic indicators of hospitalized patients with systemic lupus erythematosus: a large retrospective multicenter study in China. J Rheumatol:1289–1295

  22. 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 33:57–63

    Article  PubMed  Google Scholar 

  23. 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 64:159–168

    Article  Google Scholar 

  24. Tan EM, Cohen AS, Fries JF, Masi AT, Mcshane DJ, Rothfield NF et al (1982) The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum:1271–1277

  25. Hochberg MC (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum:1725

  26. Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH (1992) Derivation of the SLEDAI. A disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. Arthritis Rheum:630–640

  27. Mok CC, Kwok CL, Ho LY, Chan PT, Yip SF (2011) Life expectancy, standardized mortality ratios, and causes of death in six rheumatic diseases in Hong Kong, China. Arthritis Rheum:1182–1189

  28. Feng X, Pan W, Liu L, Wu M, Ding F, Hu H et al (2016) Prognosis for hospitalized patients with systemic lupus erythematosus in China: 5-year update of the Jiangsu cohort. PloS One:e0168619

  29. Kang KY, Kwok SK, Ju JH, Park KS, Cho CS, Kim HY et al (2011) The causes of death in Korean patients with systemic lupus erythematosus over 11 years. Lupus:989–997

  30. Danza A, Ruiz-Irastorza G (2013) Infection risk in systemic lupus erythematosus patients: susceptibility factors and preventive strategies. Lupus. p. 1286-94

  31. Yee CS, Su L, Toescu V, Hickman R, Situnayake D, Bowman S et al (2015) Birmingham SLE cohort: outcomes of a large inception cohort followed for up to 21 years. Rheumatology:836–843

  32. Gustafsson JT, Svenungsson E (2014) Definitions of and contributions to cardiovascular disease in systemic lupus erythematosus. Autoimmunity:67–76

  33. Townsend N, Wilson L, Bhatnagar P, Wickramasinghe K, Rayner M, Nichols M (2016) Cardiovascular disease in Europe: epidemiological update 2016. Eur Heart J 37:3232–3245

    Article  PubMed  Google Scholar 

  34. De Fatima Marinho De Souza M, Gawryszewski VP, Ordunez P, Sanhueza A, Espinal MA (2012) Cardiovascular disease mortality in the Americas: current trends and disparities. Heart:1207–1212

  35. Weiwei C, Runlin G, Lisheng L, Manlu Z, Wen W, Yongjun W, Zhaosu W, Huijun L, Zhe Z, Lixin J, Shengshou H (2016) Outline of the report on cardiovascular diseases in China, 2014. Eur Heart J Suppl 18:F2–F11

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We express our gratitude to the participants for data collection. We appreciate the precious suggestions for revision in our study.

Funding

This study was supported by National Natural Science Foundation of China (81671589 and 81502016).

Author information

Author notes

  1. Xin-yao Wu, Min Yang, Yue-sheng Xie, Wei-guo Xiao, Jin Lin, Bin Zhou, Xin Guan, Cai-nan Luo, Nan Che and Xing-zhen Liu contributed equally to this work.

Authors and Affiliations

  1. Department of Rheumatology and Immunology, Shanghai Jiao Tong University School of Medicine Affiliated Ruijin Hospital, No. 197 Ruijin Second Road, Huangpu District, Shanghai, 200025, China

    Xin-yao Wu, Jia-lin Teng, Xiao-bing Cheng, Jun-na Ye, Yu-tong Su, Hui Shi, Yu-feng Yin, Meng-ru Liu, Yue Sun, Qiong-Yi Hu, Zhuo-chao Zhou, Hui-hui Chi, Cheng-de Yang & Hong-lei Liu

  2. Department of Rheumatology and Immunology, Sichuan University West China Hospital, Chengdu, China

    Min Yang & Yi Liu

  3. Department of Rheumatology and Immunology, Guangdong General Hospital, Guangzhou, China

    Yue-sheng Xie & Xiao Zhang

  4. Department of Rheumatology and Immunology, The First Hospital Affiliated to China Medical University, Shenyang, China

    Wei-guo Xiao

  5. Department of Rheumatology and Immunology, Zhejiang University School of Medicine First Affiliated Hospital, Hangzhou, China

    Jin Lin

  6. Department of Rheumatology and Immunology, Sichuan People’s Hospital, Chengdu, China

    Bin Zhou

  7. Department of Rheumatology and Immunology, Second Xiangya Hospital, Changsha, China

    Xin Guan & Jin-wei Chen

  8. Department of Rheumatology and Immunology, Xinjiang Uygur People’s Hospital, No. 91 Tianchi Road, Tianshan District, Urumqi, 830001, Xinjiang Uygur Autonomous Region, China

    Cai-nan Luo & Li-jun Wu

  9. Department of Rheumatology and Immunology, Jiangsu People’s Hospital, Nanjing, China

    Nan Che & Miao-jia Zhang

  10. Department of Rheumatology and Immunology, Changhai Hospital, Shanghai, China

    Xing-zhen Liu & Dong-bao Zhao

  11. Beijing Institute of Traumatology and Orthopaedics, Beijing Jishuitan Hospital, Fourth Clinical Medical College, Peking University, Beijing, China

    Chao Wang

Authors
  1. Xin-yao Wu
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  2. Min Yang
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  3. Yue-sheng Xie
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  5. Jin Lin
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  6. Bin Zhou
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  7. Xin Guan
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  9. Nan Che
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  28. Cheng-de Yang
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  29. Li-jun Wu
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Corresponding authors

Correspondence to Cheng-de Yang, Li-jun Wu or Hong-lei Liu.

Ethics declarations

Ethics approval and consent to participate

This study was approved by the Clinical Ethics Committee of Ruijin Hospital affiliated to Shanghai Jiao Tong University School of Medicine, West China Hospital of Sichuan University, People’s Hospital of Guangdong Province, The First Hospital Affiliated to China Medical University, The First Hospital Affiliated to Zhejiang University, People’s Hospital of Sichuan Province, The Second Xiangya Hospital of Central South University, People’s Hospital of Xinjiang Uygur Autonomous Region, People’s Hospital of Jiangsu Province, and Changhai Hospital.

Consent for publication

Written consents to publication from the participants to report individual patient data were obtained. All necessary consents from any patients or parents of the patients (children) involved in the study, including consent to participate in the study where appropriate were obtained.

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None.

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Wu, Xy., Yang, M., Xie, Ys. et al. Causes of death in hospitalized patients with systemic lupus erythematosus: a 10-year multicenter nationwide Chinese cohort. Clin Rheumatol 38, 107–115 (2019). https://doi.org/10.1007/s10067-018-4259-z

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  • DOI: https://doi.org/10.1007/s10067-018-4259-z

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