Abstract
Introduction
Chronic kidney disease (CKD) is a major risk factor for overall morbidity and mortality even in lupus nephritis (LN) patients. However, less attention has been paid to the development of CKD in patients with LN. The objective of this study was to identify predictors for CKD with 35-year experience depending on newly revised guidelines for patients with LN.
Methods
We conducted a retrospective cohort study for 401 patients who visited Seoul St. Mary’s Hospital between January 1985 and December 2019. We analyzed clinical and laboratory indices, treatment response, the final renal function, and biopsy findings. The timing and cumulative risk of developing CKD were identified by Kaplan–Meier methods. Independent risk factors for developing CKD were examined by Cox proportional hazard regression analyses.
Results
The median follow-up time after the diagnosis of LN was 131 months. CKD occurred in 15.5% of patients within 10 years after the diagnosis of LN. The development of CKD was associated with delayed-onset LN, acute renal dysfunction at onset of LN, and failure to reach complete response (CR) at 6 or 12 months rather than histopathological findings or the severity of proteinuria at onset of LN. Cumulative incidence of progression to CKD was significantly higher in patients with the three predictors mentioned above.
Conclusion
Ten-year cumulative incidence of CKD was about 15%. Our results showed that delayed-onset LN, acute renal dysfunction at the onset of LN, and inadequate treatment response assessed at 6 or 12 months after treatment were predictors for the development of CKD in LN.
Key Points • CKD is a major risk factor for overall morbidity and mortality in LN patients. • Ten-year cumulative incidence of CKD was about 15% • Delayed-onset LN, acute renal dysfunction at the onset of LN, and inadequate treatment response assessed at 6 or 12 months after treatment were predictors for the development of CKD in LN. |
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Data availability
The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.
Code availability
Not applicable.
References
Borchers AT, Leibushor N, Naguwa SM, Cheema GS, Shoenfeld Y, Gershwin ME (2012) Lupus nephritis: a critical review. Autoimmun Rev 12:174–194. https://doi.org/10.1016/j.autrev.2012.08.018
Sterner RM, Hartono SP, Grande JP (2014) The pathogenesis of lupus nephritis. J Clin Cell Immunol 5:205. https://doi.org/10.4172/2155-9899.1000205
Stenvinkel P (2010) Chronic kidney disease: a public health priority and harbinger of premature cardiovascular disease. J Intern Med 268:456–467. https://doi.org/10.1111/j.1365-2796.2010.02269.x
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 18:733–737. https://doi.org/10.1016/j.autrev.2019.05.011
Moon SJ, Kwok SK, Ju JH, Park KS, Park SH, Cho CS, Kim HY (2011) Predictors of chronic kidney disease in Korean patients with lupus nephritis. J Rheumatol 38:2588–2597. https://doi.org/10.3899/jrheum.110363
Reich HN, Gladman DD, Urowitz MB, Bargman JM, Hladunewich MA, Lou W, Fan SC, Su J, Herzenberg AM, Cattran DC, Wither J, Landolt-Marticorena C, Scholey JW, Fortin PR (2011) Persistent proteinuria and dyslipidemia increase the risk of progressive chronic kidney disease in lupus erythematosus. Kidney Int 79:914–920. https://doi.org/10.1038/ki.2010.525
Parikh SV, Nagaraja HN, Hebert L, Rovin BH (2014) Renal flare as a predictor of incident and progressive CKD in patients with lupus nephritis. Clin J Am Soc Nephrol 9:279–284. https://doi.org/10.2215/cjn.05040513
Pokroy-Shapira E, Gelernter I, Molad Y (2014) Evolution of chronic kidney disease in patients with systemic lupus erythematosus over a long-period follow-up: a single-center inception cohort study. Clin Rheumatol 33:649–657. https://doi.org/10.1007/s10067-014-2527-0
Sui M, Ye X, Ma J, Yu C, Zhao S, Liu X, Li L, Cao J, Jia X, Xie R (2015) Epidemiology and risk factors for chronic kidney disease in Chinese patients with biopsy-proven lupus nephritis. Intern Med J 45:1167–1172. https://doi.org/10.1111/imj.12840
Park DJ, Kang JH, Lee JW, Lee KE, Kim TJ, Park YW, Lee JS, Choi YD, Lee SS (2017) Risk factors to predict the development of chronic kidney disease in patients with lupus nephritis. Lupus 26:1139–1148. https://doi.org/10.1177/0961203317694257
Moroni G, Gatto M, Tamborini F, Quaglini S, Radice F, Saccon F, Frontini G, Alberici F, Sacchi L, Binda V, Trezzi B, Vaglio A, Messa P, Sinico RA, Doria A (2020) Lack of EULAR/ERA-EDTA response at 1 year predicts poor long-term renal outcome in patients with lupus nephritis. Ann Rheum Dis 79:1077–1083. https://doi.org/10.1136/annrheumdis-2020-216965
Bertsias GK, Tektonidou M, Amoura Z, Aringer M, Bajema I, Berden JH, Boletis J, Cervera R, Dörner T, Doria A, Ferrario F, Floege J, Houssiau FA, Ioannidis JP, Isenberg DA, Kallenberg CG, Lightstone L, Marks SD, Martini A, Moroni G, Neumann I, Praga M, Schneider M, Starra A, Tesar V, Vasconcelos C, van Vollenhoven RF, Zakharova H, Haubitz M, Gordon C, Jayne D, Boumpas DT (2012) Joint European League Against Rheumatism and European Renal Association-European Dialysis and Transplant Association (EULAR/ERA-EDTA) recommendations for the management of adult and paediatric lupus nephritis. Ann Rheum Dis 71:1771–1782. https://doi.org/10.1136/annrheumdis-2012-201940
Fanouriakis A, Kostopoulou M, Cheema K, Anders HJ, Aringer M, Bajema I, Boletis J, Frangou E, Houssiau FA, Hollis J, Karras A, Marchiori F, Marks SD, Moroni G, Mosca M, Parodis I, Praga M, Schneider M, Smolen JS, Tesar V, Trachana M, van Vollenhoven RF, Voskuyl AE, Teng YKO, van Leew B, Bertsias G, Jayne D, Boumpas DT (2020) 2019 Update of the Joint European League Against Rheumatism and European Renal Association-European Dialysis and Transplant Association (EULAR/ERA-EDTA) recommendations for the management of lupus nephritis. Ann Rheum Dis 79:713–723. https://doi.org/10.1136/annrheumdis-2020-216924
Hochberg MC (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 40:1725. https://doi.org/10.1002/art.1780400928
Levey AS, Eckardt KU, Tsukamoto Y, Levin A, Coresh J, Rossert J, De Zeeuw D, Hostetter TH, Lameire N, Eknoyan G (2005) Definition and classification of chronic kidney disease: a position statement from Kidney Disease: Improving Global Outcomes (KDIGO). Kidney Int 67:2089–2100. https://doi.org/10.1111/j.1523-1755.2005.00365.x
Churg J, Sobin LH (1982) Renal disease classification and atlas of glomerular disease. Igaku-Shoin, Tokyo
Weening JJ, D’Agati VD, Schwartz MM, Seshan SV, Alpers CE, Appel GB, Balow JE, Bruijn JA, Cook T, Ferrario F, Fogo AB, Ginzler EM, Hebert L, Hill G, Hill P, Jennette JC, Kong NC, Lesavre P, Lockshin M, Looi LM, Makino H, Moura LA, Nagata M (2004) The classification of glomerulonephritis in systemic lupus erythematosus revisited. Kidney Int 65:521–530. https://doi.org/10.1111/j.1523-1755.2004.00443.x
Austin HA 3rd, Muenz LR, Joyce KM, Antonovych TA, Kullick ME, Klippel JH, Decker JL, Balow JE (1983) Prognostic factors in lupus nephritis. Contribution of renal histologic data. Am J Med 75:382–391. https://doi.org/10.1016/0002-9343(83)90338-8
Faurschou M, Starklint H, Halberg P, Jacobsen S (2006) Prognostic factors in lupus nephritis: diagnostic and therapeutic delay increases the risk of terminal renal failure. J Rheumatol 33:1563–1569
Faurschou M, Dreyer L, Kamper AL, Starklint H, Jacobsen S (2010) Long-term mortality and renal outcome in a cohort of 100 patients with lupus nephritis. Arthritis Care Res (Hoboken) 62:873–880. https://doi.org/10.1002/acr.20116
Costenbader KH, Desai A, Alarcón GS, Hiraki LT, Shaykevich T, Brookhart MA, Massarotti E, Lu B, Solomon DH, Winkelmayer WC (2011) Trends in the incidence, demographics, and outcomes of end-stage renal disease due to lupus nephritis in the US from 1995 to 2006. Arthritis Rheum 63:1681–1688. https://doi.org/10.1002/art.30293
Pakchotanon R, Gladman DD, Su J, Urowitz MB (2018) Sustained complete renal remission is a predictor of reduced mortality, chronic kidney disease and end-stage renal disease in lupus nephritis. Lupus 27:468–474. https://doi.org/10.1177/0961203317726376
Naiker IP, Chrystal V, Randeree IG, Seedat YK (1997) The significance of arterial hypertension at the onset of clinical lupus nephritis. Postgrad Med J 73:230–233. https://doi.org/10.1136/pgmj.73.858.230
Cunha C, Alexander S, Ashby D, Lee J, Chusney G, Cairns TD, Lightstone L (2018) Hydroxycloroquine blood concentration in lupus nephritis: a determinant of disease outcome? Nephrol Dial Transplant 33:1604–1610. https://doi.org/10.1093/ndt/gfx318
Wu CY, Tan M, Huang JY, Chiou JY, Wei JC (2020) Hydroxychloroquine is neutral in risk of chronic kidney disease in patients with systemic lupus erythematosus. Ann Rheum Dis. https://doi.org/10.1136/annrheumdis-2020-217728
Park DJ, Choi SE, Xu H, Kang JH, Lee JS, Choi YD, Lee SS (2021) Uric acid as a risk factor for progression to chronic kidney disease in patients with lupus nephritis: results from the KORNET registry. Clin Exp Rheumatol 39:947–954
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All authors were involved in drafting the article or revising it critically for important intellectual content, and all authors read and approved the final version of the article. Study conception and design: SJM, SKK; execution of data: JL, JHJ, WUK, SHP, SKK; analysis and interpretation of data: HJ, SJM, SKK; drafting of the article: HJ, SJM, SKK.
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This study was carried out in accordance with the Helsinki Declaration and was approved by the Institutional Review Board of Seoul St. Mary’s Hospital, the Catholic University of Korea (KC21RASI0046). Since this study is a retrospective study, informed patient consent was waived.
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Jeon, H., Lee, J., Ju, J.H. et al. Chronic kidney disease in Korean patients with lupus nephritis: over a 35-year period at a single center. Clin Rheumatol 41, 1665–1674 (2022). https://doi.org/10.1007/s10067-021-06030-w
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DOI: https://doi.org/10.1007/s10067-021-06030-w