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Creatinine clearance rate predicts prognosis of patients with systemic lupus erythematosus: a large retrospective cohort study

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Abstract

Objective

To explore the association between the creatinine clearance rate (Ccr) and the prognosis of patients, and compared with estimated glomerular filtration rate (eGFR).

Methods

We retrospectively collected information of patients with SLE who were first hospitalized between 1999 and 2009 in Jiangsu Province, China, and followed up in 2010 and 2015. Ccr was calculated and dichotomized into normal group (Ccr ≥ 70) and decreasing group (Ccr < 70). The clinical characteristics of the two groups were compared and Cox proportional-hazards regression models were used to calculate hazard ratio (HR) and 95% confidence interval (CI).

Results

Among 1990 SLE patients, we observed 437 (22.0%) with decreased Ccr, including 237 cases (11.9%) with mild renal dysfunction, 136 cases (6.8%) with moderate renal dysfunction, and 64 cases (3.2%) with severe renal dysfunction. Compared to normal Ccr, decreasing Ccr had a higher risk for mortality with adjusted HR (95% CI) of 2.21 (1.59–3.06). Dose-response relationships were significantly found between increased mortality of SLE and decreased Ccr (p for trend < 0. 001), as well as eGFR. Positive associations were consistently observed in subgroups, such as systemic lupus disease activity index (SLEDAI) ≥ 15, without comorbidities and abnormal laboratory indexes. Decreasing Ccr was positively associated with mortality from infection and renal failure with HR (95% CI) of 1.80 (1.02–3.19) and 6.84 (3.05–15.36).

Conclusions

A significant association has been observed between decreased Ccr and increased risk for mortality of SLE patients. Early clinical interventions to modulate the Ccr of SLE patients may be beneficial to their survival.

Key points

• Decreasing creatinine clearance rate (Ccr) was positively associated with an overall mortality of SLE patients, with a dose-response relationship.

• Moreover, decreasing Ccr was associated with elevated mortality primarily due to infection and renal failure.

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The raw data required to reproduce these findings cannot be shared at this time as the data also forms part of other ongoing studies.

References

  1. Park SY, Joo YB, Shim J, Sung YK, Bae SC (2015) Direct medical costs and their predictors in South Korean patients with systemic lupus erythematosus. Rheumatol Int 35(11):1809–1815. https://doi.org/10.1007/s00296-015-3344-8

    Article  CAS  PubMed  Google Scholar 

  2. Serrano-Aguilar P, Trujillo-Martin Mdel M, Perez de la Rosa A, Cuellar-Pompa L, Saavedra-Medina H, Linertova R, Perestelo-Perez L, Perez-Ramos J, Rivero-Santana A, Spanish SLECPGDG (2015) Patient participation in a clinical guideline development for systemic lupus erythematosus. Patient Educ Couns 98(9):1156–1163. https://doi.org/10.1016/j.pec.2015.05.022

    Article  PubMed  Google Scholar 

  3. Feng X, Pan W, Liu L, Wu M, Ding F, Hu H, Ding X, Wei H, Zou Y, Qian X, Wang M, Wu J, Tao J, Tan J, Da Z, Zhang M, Li J, Sun L, Jiangsu Lupus Collaborative G (2016) Prognosis for hospitalized patients with systemic lupus erythematosus in China: 5-year update of the Jiangsu cohort. PLoS One 11(12):e0168619. https://doi.org/10.1371/journal.pone.0168619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Wang Z, Li M, Wang Y, Xu D, Wang Q, Zhang S, Zhao J, Su J, Wu Q, Shi Q, Leng X, Zhang W, Tian X, Zhao Y, Zeng X (2018) Long-term mortality and morbidity of patients with systemic lupus erythematosus: a single-center cohort study in China. Lupus 27(5):864–869. https://doi.org/10.1177/0961203317751852

    Article  CAS  PubMed  Google Scholar 

  5. Mak A, Cheung MW, Chiew HJ, Liu Y, Ho RC (2012) 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(6):830–839. https://doi.org/10.1016/j.semarthrit.2011.11.002

    Article  PubMed  Google Scholar 

  6. Wada Y, Hasegawa H, Saeki T, Ito S, Kuroda T, Nakano M, Narita I (2018) Long-term prognosis and factors associated with damage accrual in Japanese patients with systemic lupus erythematosus. Clin Exp Nephrol 22(3):597–602. https://doi.org/10.1007/s10157-017-1491-9

    Article  PubMed  Google Scholar 

  7. Wang Z, Wang Y, Zhu R, Tian X, Xu D, Wang Q, Wu C, Zhang S, Zhao J, Zhao Y, Li M, Zeng X (2015) Long-term survival and death causes of systemic lupus erythematosus in China: a systemic review of observational studies. Medicine (Baltimore) 94(17):e794. https://doi.org/10.1097/MD.0000000000000794

    Article  CAS  Google Scholar 

  8. 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 (2019) Causes of death in hospitalized patients with systemic lupus erythematosus: a 10-year multicenter nationwide Chinese cohort. Clin Rheumatol 38(1):107–115. https://doi.org/10.1007/s10067-018-4259-z

    Article  PubMed  Google Scholar 

  9. 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

    Article  PubMed  Google Scholar 

  10. Gladman DD, Urowitz MB, Goldsmith CH, Fortin P, Ginzler E, Gordon C, Hanly JG, Isenberg DA, Kalunian K, Nived O, Petri M, Sanchez-Guerrero J, Snaith M, Sturfelt G (1997) The reliability of the Systemic Lupus International Collaborating Clinics/American College of Rheumatology Damage Index in patients with systemic lupus erythematosus. Arthritis Rheum 40(5):809–813. https://doi.org/10.1002/art.1780400506

    Article  CAS  PubMed  Google Scholar 

  11. Isenberg DA, Rahman A, Allen E, Farewell V, Akil M, Bruce IN, D’Cruz D, Griffiths B, Khamashta M, Maddison P, McHugh N, Snaith M, Teh LS, Yee CS, Zoma A, Gordon C (2005) 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(7):902–906. https://doi.org/10.1093/rheumatology/keh624

    Article  CAS  Google Scholar 

  12. Lin J, Knight EL, Hogan ML, Singh AK (2003) A comparison of prediction equations for estimating glomerular filtration rate in adults without kidney disease. J Am Soc Nephrol 14(10):2573–2580. https://doi.org/10.1097/01.asn.0000088721.98173.4b

    Article  PubMed  Google Scholar 

  13. Zuo L, Ma YC, Zhou YH, Wang M, Xu GB, Wang HY (2005) Application of GFR-estimating equations in Chinese patients with chronic kidney disease. Am J Kidney Dis 45(3):463–472. https://doi.org/10.1053/j.ajkd.2004.11.012

    Article  PubMed  Google Scholar 

  14. Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF 3rd, Feldman HI, Kusek JW, Eggers P, Van Lente F, Greene T, Coresh J, Ckd EPI (2009) A new equation to estimate glomerular filtration rate. Ann Intern Med 150(9):604–612. https://doi.org/10.7326/0003-4819-150-9-200905050-00006

    Article  PubMed  PubMed Central  Google Scholar 

  15. Shlipak MG, Matsushita K, Arnlov J, Inker LA, Katz R, Polkinghorne KR, Rothenbacher D, Sarnak MJ, Astor BC, Coresh J, Levey AS, Gansevoort RT, Consortium CKDP (2013) Cystatin C versus creatinine in determining risk based on kidney function. N Engl J Med 369(10):932–943. https://doi.org/10.1056/NEJMoa1214234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Cockcroft DW, Gault MH (1976) Prediction of creatinine clearance from serum creatinine. Nephron 16(1):31–41. https://doi.org/10.1159/000180580

    Article  CAS  PubMed  Google Scholar 

  17. National Kidney F (2002) K/DOQI clinical practice guidelines for chronic kidney disease: evaluation, classification, and stratification. Am J Kidney Dis 39(2 Suppl 1):S1–S266. https://doi.org/10.1111/j.1745-7599.2002.tb00119.x

  18. 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. https://doi.org/10.1002/art.1780251101

    Article  CAS  PubMed  Google Scholar 

  19. Hochberg MC (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 40(9):1725. https://doi.org/10.1002/art.1780400928

    Article  CAS  PubMed  Google Scholar 

  20. 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 35(6):630–640. https://doi.org/10.1002/art.1780350606

    Article  CAS  PubMed  Google Scholar 

  21. 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(7):947–953. https://doi.org/10.1007/s10067-014-2596-0

    Article  PubMed  Google Scholar 

  22. Mageau A, Timsit JF, Perrozziello A, Ruckly S, Dupuis C, Bouadma L, Papo T, Sacre K (2019) The burden of chronic kidney disease in systemic lupus erythematosus: A nationwide epidemiologic study. Autoimmun Rev 18(7):733–737. https://doi.org/10.1016/j.autrev.2019.05.011

    Article  PubMed  Google Scholar 

  23. Hanly JG, O’Keeffe AG, Su L, Urowitz MB, Romero-Diaz J, Gordon C, Bae SC, Bernatsky S, Clarke AE, Wallace DJ, Merrill JT, Isenberg DA, Rahman A, Ginzler EM, Fortin P, Gladman DD, Sanchez-Guerrero J, Petri M, Bruce IN, Dooley MA, Ramsey-Goldman R, Aranow C, Alarcon GS, Fessler BJ, Steinsson K, Nived O, Sturfelt GK, Manzi S, Khamashta MA, van Vollenhoven RF, Zoma AA, Ramos-Casals M, Ruiz-Irastorza G, Lim SS, Stoll T, Inanc M, Kalunian KC, Kamen DL, Maddison P, Peschken CA, Jacobsen S, Askanase A, Theriault C, Thompson K, Farewell V (2016) The frequency and outcome of lupus nephritis: results from an international inception cohort study. Rheumatology (Oxford) 55(2):252–262. https://doi.org/10.1093/rheumatology/kev311

    Article  Google Scholar 

  24. Thomas G, Mancini J, Jourde-Chiche N, Sarlon G, Amoura Z, Harle JR, Jougla E, Chiche L (2014) Mortality associated with systemic lupus erythematosus in France assessed by multiple-cause-of-death analysis. Arthritis Rheum 66(9):2503–2511. https://doi.org/10.1002/art.38731

    Article  Google Scholar 

  25. Yee CS, Su L, Toescu V, Hickman R, Situnayake D, Bowman S, Farewell V, Gordon C (2015) Birmingham SLE cohort: outcomes of a large inception cohort followed for up to 21 years. Rheumatology (Oxford) 54(5):836–843. https://doi.org/10.1093/rheumatology/keu412

    Article  CAS  Google Scholar 

  26. James MT, Laupland KB, Tonelli M, Manns BJ, Culleton BF, Hemmelgarn BR, Network AKD (2008) Risk of bloodstream infection in patients with chronic kidney disease not treated with dialysis. Arch Intern Med 168(21):2333–2339. https://doi.org/10.1001/archinte.168.21.2333

    Article  PubMed  Google Scholar 

  27. James MT, Quan H, Tonelli M, Manns BJ, Faris P, Laupland KB, Hemmelgarn BR, Alberta Kidney Disease N (2009) CKD and risk of hospitalization and death with pneumonia. Am J Kidney Dis 54(1):24–32. https://doi.org/10.1053/j.ajkd.2009.04.005

    Article  PubMed  Google Scholar 

  28. Dalrymple LS, Katz R, Kestenbaum B, de Boer IH, Fried L, Sarnak MJ, Shlipak MG (2012) The risk of infection-related hospitalization with decreased kidney function. Am J Kidney Dis 59(3):356–363. https://doi.org/10.1053/j.ajkd.2011.07.012

    Article  PubMed  Google Scholar 

  29. Nakayama M, Metoki H, Terawaki H, Ohkubo T, Kikuya M, Sato T, Nakayama K, Asayama K, Inoue R, Hashimoto J, Totsune K, Hoshi H, Ito S, Imai Y (2007) Kidney dysfunction as a risk factor for first symptomatic stroke events in a general japanese population--the Ohasama study. Nephrol Dial Transplant 22(7):1910–1915

    Article  PubMed  Google Scholar 

  30. Suzuki M, Ross GF, Wiers K, Nelson S, Bennett M, Passo MH, Devarajan P, Brunner HI (2007) Identification of a urinary proteomic signature for lupus nephritis in children. Pediatr Nephrol 22(12):2047–2057. https://doi.org/10.1007/s00467-007-0608-x

    Article  PubMed  Google Scholar 

  31. Mosley K, Tam FW, Edwards RJ, Crozier J, Pusey CD, Lightstone L (2006) Urinary proteomic profiles distinguish between active and inactive lupus nephritis. Rheumatology 45(12):1497–1504. https://doi.org/10.1093/rheumatology/kel351

    Article  CAS  PubMed  Google Scholar 

  32. Yu F, Tan Y, Liu G, Wang SX, Zou WZ, Zhao MH (2009) Clinicopathological characteristics and outcomes of patients with crescentic lupus nephritis. Kidney Int 76(3):307–317. https://doi.org/10.1038/ki.2009.136

    Article  PubMed  Google Scholar 

  33. López-Pelayo I, Mazuecos Blanca MA, García Palacios MV, Galán Sánchez F, López Rodríguez F, Bailén García MA (2019) How to manage kidney transplant recipients: deciding between glomerular filtration rate-estimating equations, creatinine clearance and albumin-creatinine ratio, or albumin excretion. Exp Clin Transplant 17(4):450–456. https://doi.org/10.6002/ect.2017.0335

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank all investigators and site staff of local hospitals who participated in this study and the Cinkate Corp for their assistance in helping built and manage our database website.

Funding

This work was supported by the Major International (Regional) Joint Research Project of China (No. 81720108020) and the Key Program of the National Natural Science Foundation of China (No. 81930043).

Author information

Author notes

  1. Jiahuan Ge and Ziyi Jin contributed equally as first authors.

  2. Ziyi Jin and Lingyun Sun contributed equally as senior authors.

Authors and Affiliations

  1. Nanjing Drum Tower Hospital Clinical College, Nanjing Medical University, Nanjing, China

    Jiahuan Ge & Lingyun Sun

  2. Department of Rheumatology and Immunology, The Affiliated Drum Tower Hospital, Nanjing University Medical School, 321 Zhongshan Road, Nanjing, 210008, China

    Ziyi Jin, Xuebing Feng & Lingyun Sun

  3. Department of Rheumatology, Huai’an First People’s Hospital, Huai’an, China

    Wenyou Pan

  4. Department of Rheumatology, Xuzhou Central Hospital, Xuzhou, China

    Lin Liu

  5. Department of Rheumatology, The Third Affiliated Hospital of Soochow University, Changzhou, China

    Min Wu

  6. Department of Rheumatology, Lianyungang Second People’s Hospital, Lianyungang, China

    Huaixia Hu

  7. Department of Rheumatology, Lianyungang First People’s Hospital, Lianyungang, China

    Xiang Ding

  8. Department of Rheumatology, Northern Jiangsu People’s Hospital, Yangzhou, China

    Hua Wei

  9. Department of Rheumatology, Wuxi People’s Hospital, Wuxi, China

    Yaohong Zou

  10. Department of Rheumatology, Jiangsu Province Hospital of TCM, Nanjing, China

    Xian Qian

  11. Department of Rheumatology, Southeast University Zhongda Hospital, Nanjing, China

    Meimei Wang

  12. Department of Rheumatology, The First Affiliated Hospital of Soochow University, Suzhou, China

    Jian Wu

  13. Department of Rheumatology, Wuxi TCM Hospital, Wuxi, China

    Juan Tao

  14. Department of Rheumatology, Zhenjiang First People’s Hospital, Zhenjiang, China

    Jun Tan

  15. Department of Rheumatology, Affiliated Hospital of Nantong University, Nantong, China

    Zhanyun Da

  16. Department of Rheumatology, Jiangsu Province Hospital, Nanjing, China

    Miaojia Zhang

  17. Department of Rheumatology, Affiliated Hospital of Jiangsu University, Zhenjiang, Jiangsu, China

    Jing Li

Authors
  1. Jiahuan Ge
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  2. Ziyi Jin
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  3. Xuebing Feng
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  4. Wenyou Pan
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  5. Lin Liu
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  6. Min Wu
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  7. Huaixia Hu
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  8. Xiang Ding
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  9. Hua Wei
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  10. Yaohong Zou
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  11. Xian Qian
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  12. Meimei Wang
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  15. Jun Tan
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  16. Zhanyun Da
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  17. Miaojia Zhang
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  18. Jing Li
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  19. Lingyun Sun
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Contributions

Study conception and design: J.G., Z.J., L.S. Acquisition of data: X.F., W.P., L.L., Min W., H.H., X.D., H.W., Y.Z., X.Q., Meimei W., J.W., Juan T., Jun T., Z.D., M.Z., J.L., L.S. Analysis and drafting the article: J.G., Z.J. Revising the article: Z.J., L.S. All authors have finally approved the submitted version to be published.

Corresponding authors

Correspondence to Ziyi Jin or Lingyun Sun.

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Ge, J., Jin, Z., Feng, X. et al. Creatinine clearance rate predicts prognosis of patients with systemic lupus erythematosus: a large retrospective cohort study. Clin Rheumatol 40, 2221–2231 (2021). https://doi.org/10.1007/s10067-020-05485-7

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