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Analysis of clinical and laboratory characteristics and pathology of lupus nephritis-based on 710 renal biopsies in China

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Abstract

Objectives

This study aimed to analyse the clinical and laboratory characteristics of different pathologic classifications of lupus nephritis (LN) patients in terms of age at systemic lupus erythematosus (SLE) diagnosis and nephritis onset.

Method

Clinical, laboratory, and pathological data of 710 LN patients diagnosed by renal biopsy at our institution between 2000 and 2018 were retrospectively analysed. Patients were divided into the different pathological classification groups; childhood-, adult- and elderly-onset SLE groups and early- and late-onset LN groups.

Results

Class IV occurred most frequently and had the lowest complement C3 level. There was an obvious increase in active index in class IV and class V + IV. Patients with class VI showed some clinical characteristics similar to end-stage renal disease. Patients with proliferative nephritis were younger at SLE diagnosis and had higher blood pressure, higher frequency of proteinuria and urinary erythrocyte and lower haemoglobin and complement C3. Pathologic classification between childhood-, adult- and elderly-onset SLE patients or between early- and late-onset LN patients was not significantly different. Elderly-onset SLE patients had the highest chronic index (CI), IgA, IgG and Sjögren’s syndrome A antibodies and Sjögren’s syndrome B antibodies rates, whereas late-onset LN patients showed significantly higher CI, haemoglobin, complement C3 and C4 but lower uric acid, IgM and IgG.

Conclusions

LN patients present with different clinical and laboratory characteristics according to pathological classification, age at SLE diagnosis and nephritis onset. These results might be valuable for estimating the pathology and guiding treatment and prognosis.

Key Points

• Patients with proliferative nephritis have more severe immune disorders, worse renal function and stronger inflammatory state.

• The elderly-onset SLE patients showed a poorer condition.

• The late-onset LN patients might have a more stable status.

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References

  1. Lisnevskaia L, Murphy G, Isenberg D (2014) Systemic lupus erythematosus. Lancet 384(9957):1878–1888. https://doi.org/10.1016/S0140-6736(14)60128-8

    Article  PubMed  Google Scholar 

  2. Lessard CJ, Sajuthi S, Zhao J, Kim K, Ice JA, Li H, Ainsworth H, Rasmussen A, Kelly JA, Marion M, Bang SY, Joo YB, Choi J, Lee HS, Kang YM, Suh CH, Chung WT, Lee SK, Choe JY, Shim SC, Oh JH, Kim YJ, Han BG, Shen N, Howe HS, Wakeland EK, Li QZ, Song YW, Gaffney PM, Alarcon-Riquelme ME, Criswell LA, Jacob CO, Kimberly RP, Vyse TJ, Harley JB, Sivils KL, Bae SC, Langefeld CD, Tsao BP (2016) Identification of a systemic lupus erythematosus risk locus spanning ATG16L2, FCHSD2, and P2RY2 in Koreans. Arthritis Rheumatol 68(5):1197–1209. https://doi.org/10.1002/art.39548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Niu Z, Zhang P, Tong Y (2015) Value of HLA-DR genotype in systemic lupus erythematosus and lupus nephritis: a meta-analysis. Int J Rheum Dis 18(1):17–28. https://doi.org/10.1111/1756-185X.12528

    Article  CAS  PubMed  Google Scholar 

  4. Bertsias GK, Boumpas DT (2011) Connective tissue diseases: lupus nephritis-winning a few battles but not the war. Nat Rev Rheumatol 7(8):441–442. https://doi.org/10.1038/nrrheum.2011.88

    Article  PubMed  Google Scholar 

  5. Maroz N, Segal MS (2013) Lupus nephritis and end-stage kidney disease. Am J Med Sci 346(4):319–323. https://doi.org/10.1097/MAJ.0b013e31827f4ee3

    Article  PubMed  Google Scholar 

  6. Lydia A, Saraswati MH, Dharmeizar D, Saraswati M, Setiati S (2018) Diagnostic determinants of proliferative lupus nephritis based on clinical and laboratory parameters: a diagnostic study. Acta Med Indones 50(2):110–118

    PubMed  Google Scholar 

  7. 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, International Society of Nephrology Working Group on the Classification of Lupus N, Renal Pathology Society Working Group on the Classification of Lupus N (2004) The classification of glomerulonephritis in systemic lupus erythematosus revisited. Kidney Int 65(2):521–530. https://doi.org/10.1111/j.1523-1755.2004.00443.x

    Article  PubMed  Google Scholar 

  8. Chen DN, Fan L, Wu YX, Zhou Q, Chen W, Yu XQ (2018) A predictive model for estimation risk of proliferative lupus nephritis. Chin Med J 131(11):1275–1281. https://doi.org/10.4103/0366-6999.232809

    Article  PubMed  PubMed Central  Google Scholar 

  9. Tang Y, Zhang W, Zhu M, Zheng L, Xie L, Yao Z, Zhang H, Cao D, Lu B (2018) Lupus nephritis pathology prediction with clinical indices. Sci Rep 8(1):10231. https://doi.org/10.1038/s41598-018-28611-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Bomback AS (2018) An update on therapies for proliferative lupus nephritis: how certain can we be about the evidence? Am J Kidney Dis 72(5):758–760. https://doi.org/10.1053/j.ajkd.2018.07.007

    Article  PubMed  Google Scholar 

  11. Yokoyama H, Wada T, Hara A, Yamahana J, Nakaya I, Kobayashi M, Kitagawa K, Kokubo S, Iwata Y, Yoshimoto K, Shimizu K, Sakai N, Furuichi K, Kanazawa Study Group for Renal D, Hypertension (2004) The outcome and a new ISN/RPS 2003 classification of lupus nephritis in Japanese. Kidney Int 66(6):2382–2388. https://doi.org/10.1111/j.1523-1755.2004.66027.x

    Article  PubMed  Google Scholar 

  12. Schwartz N, Goilav B, Putterman C (2014) The pathogenesis, diagnosis and treatment of lupus nephritis. Curr Opin Rheumatol 26(5):502–509. https://doi.org/10.1097/BOR.0000000000000089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Antolin J, Amerigo MJ, Cantabrana A, Roces A, Jimenez P (1995) Systemic lupus erythematosus: clinical manifestations and immunological parameters in 194 patients. Subgroup classification of SLE. Clin Rheumatol 14(6):678–685. https://doi.org/10.1007/bf02207936

    Article  CAS  PubMed  Google Scholar 

  14. Klein-Gitelman M, Reiff A, Silverman ED (2002) Systemic lupus erythematosus in childhood. Rheum Dis Clin N Am 28(3):561–577 vi-vii

    Article  Google Scholar 

  15. Tomic-Lucic A, Petrovic R, Radak-Perovic M, Milovanovic D, Milovanovic J, Zivanovic S, Pantovic S, Veselinovic M (2013) Late-onset systemic lupus erythematosus: clinical features, course, and prognosis. Clin Rheumatol 32(7):1053–1058. https://doi.org/10.1007/s10067-013-2238-y

    Article  PubMed  Google Scholar 

  16. das Chagas Medeiros MM, Bezerra MC, Braga FN, da Justa Feijao MR, Gois AC, Reboucas VC, de Carvalho TM, Carvalho LN, Ribeiro AM (2016) Clinical and immunological aspects and outcome of a Brazilian cohort of 414 patients with systemic lupus erythematosus (SLE): comparison between childhood-onset, adult-onset, and late-onset SLE. Lupus 25(4):355–363. https://doi.org/10.1177/0961203315606983

    Article  CAS  PubMed  Google Scholar 

  17. Seligman VA, Lum RF, Olson JL, Li H, Criswell LA (2002) Demographic differences in the development of lupus nephritis: a retrospective analysis. Am J Med 112(9):726–729. https://doi.org/10.1016/s0002-9343(02)01118-x

    Article  PubMed  Google Scholar 

  18. Kang JH, Park DJ, Lee KE, Lee JS, Choi YD, Lee SS (2017) Comparison of clinical, serological, and prognostic differences among juvenile-, adult-, and late-onset lupus nephritis in Korean patients. Clin Rheumatol 36(6):1289–1295. https://doi.org/10.1007/s10067-017-3641-6

    Article  PubMed  Google Scholar 

  19. Varela DC, Quintana G, Somers EC, Rojas-Villarraga A, Espinosa G, Hincapie ME, McCune WJ, Cervera R, Anaya JM (2008) Delayed lupus nephritis. Ann Rheum Dis 67(7):1044–1046. https://doi.org/10.1136/ard.2008.088740

    Article  PubMed  Google Scholar 

  20. Ugolini-Lopes MR, Santos LPS, Stagnaro C, Seguro LPC, Mosca M, Bonfa E (2019) Late-onset biopsy-proven lupus nephritis without other associated autoimmune diseases: severity and long-term outcome. Lupus 28(1):123–128. https://doi.org/10.1177/0961203318811603

    Article  CAS  PubMed  Google Scholar 

  21. Guo Q, Lu X, Miao L, Wu M, Lu S, Luo P (2010) Analysis of clinical manifestations and pathology of lupus nephritis: a retrospective review of 82 cases. Clin Rheumatol 29(10):1175–1180. https://doi.org/10.1007/s10067-010-1517-0

    Article  PubMed  Google Scholar 

  22. Shariati-Sarabi Z, Ranjbar A, Monzavi SM, Esmaily H, Farzadnia M, Zeraati AA (2013) Analysis of clinicopathologic correlations in Iranian patients with lupus nephritis. Int J Rheum Dis 16(6):731–738. https://doi.org/10.1111/1756-185X.12059

    Article  CAS  PubMed  Google Scholar 

  23. Satirapoj B, Tasanavipas P, Supasyndh O (2015) Clinicopathological correlation in Asian patients with biopsy-proven lupus nephritis. Int J Nephrol 2015:857316–857316. https://doi.org/10.1155/2015/857316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Silva CA, Avcin T, Brunner HI (2012) Taxonomy for systemic lupus erythematosus with onset before adulthood. Arthritis Care Res 64(12):1787–1793. https://doi.org/10.1002/acr.21757

    Article  Google Scholar 

  25. Schwartz GJ, Munoz A, Schneider MF, Mak RH, Kaskel F, Warady BA, Furth SL (2009) New equations to estimate GFR in children with CKD. J Am Soc Nephrol 20(3):629–637. https://doi.org/10.1681/ASN.2008030287

    Article  PubMed  PubMed Central  Google Scholar 

  26. Stevens LA, Claybon MA, Schmid CH, Chen J, Horio M, Imai E, Nelson RG, Van Deventer M, Wang HY, Zuo L, Zhang YL, Levey AS (2011) Evaluation of the chronic kidney disease epidemiology collaboration equation for estimating the glomerular filtration rate in multiple ethnicities. Kidney Int 79(5):555–562. https://doi.org/10.1038/ki.2010.462

    Article  PubMed  Google Scholar 

  27. Gupta R, Aggarwal A, Sinha S, Rajasekhar L, Yadav A, Gaur P, Misra R, Negi VS (2016) Urinary osteoprotegerin: a potential biomarker of lupus nephritis disease activity. Lupus 25(11):1230–1236. https://doi.org/10.1177/0961203316636470

    Article  CAS  PubMed  Google Scholar 

  28. Hiromura K, Ikeuchi H, Kayakabe K, Sugiyama H, Nagata M, Sato H, Yokoyama H, Nojima Y (2017) Clinical and histological features of lupus nephritis in Japan: a cross-sectional analysis of the Japan Renal Biopsy Registry (J-RBR). Nephrology (Carlton) 22(11):885–891. https://doi.org/10.1111/nep.12863

    Article  Google Scholar 

  29. Nossent J, Raymond W, Kang A, Wong D, Ognjenovic M, Chakera A (2018) The current role for clinical and renal histological findings as predictor for outcome in Australian patients with lupus nephritis. Lupus 27(11):1838–1846. https://doi.org/10.1177/0961203318792361

    Article  CAS  PubMed  Google Scholar 

  30. Restrepo-Escobar M, Granda-Carvajal PA, Jaimes F (2019) Development and internal validation of a prediction model to estimate the probability of needing aggressive immunosuppressive therapy with cytostatics in de novo lupus nephritis patients. Reumatol Clin 15(1):27–33. https://doi.org/10.1016/j.reuma.2017.05.010

    Article  PubMed  Google Scholar 

  31. Mitjavila F, Pac V, Moga I, Poveda R, Vidaller A, Carrera M, Pujol R (1997) Clinicopathological correlations and prognostic factors in lupus nephritis. Clin Exp Rheumatol 15(6):625–631

    CAS  PubMed  Google Scholar 

  32. Okpechi IG, Swanepoel CR, Tiffin N, Duffield M, Rayner BL (2012) Clinicopathological insights into lupus nephritis in South Africans: a study of 251 patients. Lupus 21(9):1017–1024. https://doi.org/10.1177/0961203312441981

    Article  CAS  PubMed  Google Scholar 

  33. Xu YX, Tan Y, Yu F, Zhao MH (2011) Late onset lupus nephritis in Chinese patients: classified by the 2003 International Society of Nephrology and Renal Pathology Society system. Lupus 20(8):801–808. https://doi.org/10.1177/0961203310397563

    Article  PubMed  Google Scholar 

  34. Tang Z, Chen D, Yang S, Zhang H, Hu W, Liu Z, Li L (2011) Late onset lupus nephritis: analysis of clinical manifestations and renal pathological features in Chinese patients. Rheumatol Int 31(12):1625–1629. https://doi.org/10.1007/s00296-010-1536-9

    Article  PubMed  Google Scholar 

  35. Denic A, Glassock RJ, Rule AD (2016) Structural and functional changes with the aging kidney. Adv Chronic Kidney Dis 23(1):19–28. https://doi.org/10.1053/j.ackd.2015.08.004

    Article  PubMed  PubMed Central  Google Scholar 

  36. Ruacho G, Kvarnstrom M, Zickert A, Oke V, Ronnelid J, Eketjall S, Elvin K, Gunnarsson I, Svenungsson E (2019) Sjogren's syndrome in systemic lupus erythematosus - a subset characterized by a systemic inflammatory state. J Rheumatol jrheum.190250. https://doi.org/10.3899/jrheum.190250

  37. Choi JH, Park DJ, Kang JH, Yim YR, Lee KE, Lee JW, Wen L, Kim TJ, Park YW, Lee JK, Lee SS (2015) Comparison of clinical and serological differences among juvenile-, adult-, and late-onset systemic lupus erythematosus in Korean patients. Lupus 24(12):1342–1349. https://doi.org/10.1177/0961203315591024

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was supported by the National Natural Science Foundation of China [grant number 81830019].

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Authors and Affiliations

  1. Department of Nephrology, Chinese PLA Institute of Nephrology, State Key Laboratory of Kidney Diseases, National Clinical Research Center for Kidney Diseases, Beijing Key Laboratory of Kidney Diseases, Medical School of Chinese PLA, the First Medical Centre, Chinese PLA General Hospital, 28 Fuxing Road, Beijing, China

    Kangkang Song, Xiaomin Liu, Jiaona Liu, Zhong Yin, Pu Chen, Guangyan Cai & Xiangmei Chen

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  1. Kangkang Song
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  2. Xiaomin Liu
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  7. Xiangmei Chen
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Correspondence to Xiangmei Chen.

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This study was approved by the Ethics Committee of the Chinese People’s Liberation Army General Hospital (no. S2019-095-01), and informed consent was obtained before undergoing kidney biopsy.

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Song, K., Liu, X., Liu, J. et al. Analysis of clinical and laboratory characteristics and pathology of lupus nephritis-based on 710 renal biopsies in China. Clin Rheumatol 39, 3353–3363 (2020). https://doi.org/10.1007/s10067-020-05115-2

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