Skip to main content
SpringerLink
Log in

The ratio of neutrophil to lymphocyte as a potential marker of clinicopathological activity for lupus nephritis

  • Nephrology - Original Paper
  • Published:
International Urology and Nephrology Aims and scope Submit manuscript

Abstract

Introduction

The ratio of neutrophil to lymphocyte (NLR) is a novel inflammatory factor that is elevated in systemic lupus erythematosus (SLE). However, the relationship between NLR and renal pathological manifestations in patients with lupus nephritis (LN) has not been investigated.

Methods

A retrospective study included 240 SLE patients, in which 186 patients with renal involvement and 124 LN patients underwent renal biopsy, 125 healthy volunteers and 125 chronic kidney disease (CKD) controls. Patients with SLE disease activity 2000 (SLEDAI-2 K) > 9 and ≤ 9 were defined as severely active and mildly active, respectively. Clinical parameters and renal pathological data were collected from medical records. The correlations between NLR and clinicopathological features were analyzed.

Results

The NLR of SLE group was significantly higher than that of the sex-age matched control groups. Patients with nephritis had higher NLR levels than those without nephritis (P = 0.044). Increased NLR was observed in severely active group compared to mildly active group (P = 0.020). NLR was significantly positively related with SLEDAI score, Renal SLEDAI score, C-reactive protein (CRP), 24-h urine protein, renal activity index (AI), cellular crescents and tubular atrophy, and negatively correlated with serum albumin. NLR was significantly decreased after treatment. Based on the receiver operating characteristic (ROC) curve, the best NLR cut-off value to predict severe activity of SLE and cellular crescents in renal pathology was 2.19 and 3.16, respectively.

Conclusion

NLR may be a non-invasive and potential inflammatory marker in evaluating clinical and renal pathological activity in LN patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

The datasets generated or analyzed during this study are available from the corresponding author on reasonable request.

References

  1. Tsokos GC (2020) Autoimmunity and organ damage in systemic lupus erythematosus. Nat Immunol 21(6):605–614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Kiriakidou M, Ching CL (2020) Systemic lupus erythematosus. Ann Intern Med 172(11):Itc81–Itc96

    Article  PubMed  Google Scholar 

  3. Mohan C, Putterman C (2015) Genetics and pathogenesis of systemic lupus erythematosus and lupus nephritis. Nat Rev Nephrol 11(6):329–341

    Article  CAS  PubMed  Google Scholar 

  4. Justiz Vaillant AA, Goyal A, Bansal P et al (2020) Systemic lupus erythematosus. StatPearls. Treasure Island (FL): StatPearls Publishing Copyright © 2020, StatPearls Publishing LLC

  5. Mercan R, Bitik B, Tufan A et al (2016) The association between neutrophil/lymphocyte ratio and disease activity in rheumatoid arthritis and ankylosing spondylitis. J Clin Lab Anal 30(5):597–601

    Article  CAS  PubMed  Google Scholar 

  6. Zeng Z, Wang C, Wang B et al (2019) Prediction of neutrophil-to-lymphocyte ratio in the diagnosis and progression of autoimmune encephalitis. Neurosci Lett 694:129–135

    Article  CAS  PubMed  Google Scholar 

  7. Gao MZ, Huang YL, Wu XD et al (2018) Red blood cell distribution width and neutrophil to lymphocyte ratio are correlated with disease activity of dermatomyositis and polymyositis. J Clin Lab Anal 32(1):e22209

    Article  PubMed  Google Scholar 

  8. Muñoz LE, Janko C, Schulze C et al (2010) Autoimmunity and chronic inflammation - two clearance-related steps in the etiopathogenesis of SLE. Autoimmun Rev 10(1):38–42

    Article  PubMed  Google Scholar 

  9. Wang L, Wang C, Jia X et al (2020) Relationship between neutrophil-to-lymphocyte ratio and systemic lupus erythematosus: a meta-analysis. Clinics (Sao Paulo) 75:e1450

    Article  PubMed  Google Scholar 

  10. Liang P, Tang Y, Lin L et al (2018) Low level of circulating basophil counts in biopsy-proven active lupus nephritis. Clin Rheumatol 37(2):459–465

    Article  PubMed  Google Scholar 

  11. Liang P, Tang Y, Fu S et al (2015) Basophil count, a marker for disease activity in systemic lupus erythematosus. Clin Rheumatol 34(5):891–896

    Article  PubMed  Google Scholar 

  12. Ekici H, Imamoglu M, Okmen F et al (2022) Evaluation of neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio in pregnant women with systemic lupus erythematosus. J Obstet Gynaecol 42(5):872–876

    Article  CAS  PubMed  Google Scholar 

  13. Wu Y, Chen Y, Yang X et al (2016) Neutrophil-to-lymphocyte ratio (NLR) and platelet-to-lymphocyte ratio (PLR) were associated with disease activity in patients with systemic lupus erythematosus. Int Immunopharmacol 36:94–99

    Article  CAS  PubMed  Google Scholar 

  14. Yu J, Zeng T, Wu Y et al (2019) Neutrophil-to-C3 ratio and neutrophil-to-lymphocyte ratio were associated with disease activity in patients with systemic lupus erythematosus. J Clin Lab Anal 33(1):e22633

    Article  PubMed  Google Scholar 

  15. Weening JJ, D’Agati VD, Schwartz MM et al (2004) The classification of glomerulonephritis in systemic lupus erythematosus revisited. Kidney Int 65(2):521–530

    Article  PubMed  Google Scholar 

  16. Austin HA 3rd, Muenz LR, Joyce KM et al (1983) Prognostic factors in lupus nephritis. Contribution of renal histologic data. Am J Med 75(3):382–391

    Article  PubMed  Google Scholar 

  17. Carli L, Tani C, Vagnani S et al (2015) Leukopenia, lymphopenia, and neutropenia in systemic lupus erythematosus: prevalence and clinical impact–A systematic literature review. Semin Arthritis Rheum 45(2):190–194

    Article  PubMed  Google Scholar 

  18. Hepburn AL, Narat S, Mason JC (2010) The management of peripheral blood cytopenias in systemic lupus erythematosus. Rheumatology (Oxford) 49(12):2243–2254

    Article  CAS  PubMed  Google Scholar 

  19. Denny MF, Yalavarthi S, Zhao W et al (2010) A distinct subset of proinflammatory neutrophils isolated from patients with systemic lupus erythematosus induces vascular damage and synthesizes type I IFNs. J Immunol 184(6):3284–3297

    Article  CAS  PubMed  Google Scholar 

  20. Kaplan MJ (2011) Neutrophils in the pathogenesis and manifestations of SLE. Nat Rev Rheumatol 7(12):691–699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Ren Y, Tang J, Mok MY et al (2003) Increased apoptotic neutrophils and macrophages and impaired macrophage phagocytic clearance of apoptotic neutrophils in systemic lupus erythematosus. Arthritis Rheum 48(10):2888–2897

    Article  PubMed  Google Scholar 

  22. Flesher DL, Sun X, Behrens TW et al (2010) Recent advances in the genetics of systemic lupus erythematosus. Expert Rev Clin Immunol 6(3):461–479

    Article  PubMed  PubMed Central  Google Scholar 

  23. Lu R, Robertson JM, Bruner BF et al (2012) Multiple autoantibodies display association with lymphopenia, proteinuria, and cellular casts in a large, ethnically diverse SLE patient cohort. Autoimmune Dis 2012:819634

    PubMed  PubMed Central  Google Scholar 

  24. Li C, Mu R, Lu XY et al (2014) Antilymphocyte antibodies in systemic lupus erythematosus: association with disease activity and lymphopenia. J Immunol Res 2014:672126

    Article  PubMed  PubMed Central  Google Scholar 

  25. Emlen W, Niebur J, Kadera R (1994) Accelerated in vitro apoptosis of lymphocytes from patients with systemic lupus erythematosus. J Immunol 152(7):3685–3692

    Article  CAS  PubMed  Google Scholar 

  26. Richardson BC, Yung RL, Johnson KJ et al (1996) Monocyte apoptosis in patients with active lupus. Arthritis Rheum 39(8):1432–1434

    Article  CAS  PubMed  Google Scholar 

  27. Silva LM, Garcia AB, Donadi EA (2002) Increased lymphocyte death by neglect-apoptosis is associated with lymphopenia and autoantibodies in lupus patients presenting with neuropsychiatric manifestations. J Neurol 249(8):1048–1054

    Article  PubMed  Google Scholar 

  28. Templeton AJ, McNamara MG, Šeruga B et al (2014) Prognostic role of neutrophil-to-lymphocyte ratio in solid tumors: a systematic review and meta-analysis. J Natl Cancer Inst 106(6):dju124

    Article  PubMed  Google Scholar 

  29. Erre GL, Paliogiannis P, Castagna F et al (2019) Meta-analysis of neutrophil-to-lymphocyte and platelet-to-lymphocyte ratio in rheumatoid arthritis. Eur J Clin Invest 49(1):e13037

    Article  PubMed  Google Scholar 

  30. Forget P, Khalifa C, Defour JP et al (2017) What is the normal value of the neutrophil-to-lymphocyte ratio? BMC Res Notes 10(1):12

    Article  PubMed  PubMed Central  Google Scholar 

  31. Qin B, Ma N, Tang Q et al (2016) Neutrophil to lymphocyte ratio (NLR) and platelet to lymphocyte ratio (PLR) were useful markers in assessment of inflammatory response and disease activity in SLE patients. Mod Rheumatol 26(3):372–376

    Article  PubMed  Google Scholar 

  32. Soliman WM, Sherif NM, Ghanima IM et al (2020) Neutrophil to lymphocyte and platelet to lymphocyte ratios in systemic lupus erythematosus: relation with disease activity and lupus nephritis. Rheumatol Clin 16(4):255–261

    Google Scholar 

  33. Yu H, Jiang L, Yao L et al (2018) Predictive value of the neutrophil-to-lymphocyte ratio and hemoglobin in systemic lupus erythematosus. Exp Ther Med 16(2):1547–1553

    PubMed  PubMed Central  Google Scholar 

  34. Tatar E, Mirili C, Isikyakar T et al (2016) The association of neutrophil/lymphocyte ratio and platelet/lymphocyte ratio with clinical outcomes in geriatric patients with stage 3–5 chronic kidney disease. Acta Clin Belg 71(4):221–226

    Article  PubMed  Google Scholar 

Download references

Funding

This work was supported by grants of the National Natural Science Foundation of China (No. 81770709), the Guangzhou Municipal Science and Technology Project (No. 201904010142), the Natural Science Foundation of Guangdong Province(No.2020A1515010429), and Sun Yat-sen Memorial Hospital Clinical Research and Cultivation Project (No. SYS-C-201903).

Author information

Author notes

  1. Qianqian Han and Peifen Liang have contributed equally to this work.

Authors and Affiliations

  1. Department of Nephrology, Sun Yat-sen Memorial Hospital, Sun Yat-sen University, 107 Yan Jiang West Road, Guangzhou, 510120, China

    Qianqian Han, Peifen Liang, Jiajia Li, Bo Liu, Rui Zhang, Xuefeng Xie, Yingyan Liang & Qiongqiong Yang

  2. Guangdong Provincial Key Laboratory of Malignant Tumor Epigenetics and Gene Regulation, Sun Yat-sen Memorial Hospital, Sun Yat-sen University, Guangzhou, 510120, China

    Qianqian Han, Peifen Liang, Jiajia Li, Bo Liu, Rui Zhang, Xuefeng Xie, Yingyan Liang & Qiongqiong Yang

Authors
  1. Qianqian Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peifen Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jiajia Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bo Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rui Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xuefeng Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yingyan Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Qiongqiong Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

QY: Research concept and design, final approval of article. QH: Writing the article. PL: Critical revision of the article. JL: Data analysis and interpretation. BL and RZ: Collection and assembly of patient data. XX and YL: Collection and assembly of the control group data.

Corresponding author

Correspondence to Qiongqiong Yang.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare.

Ethical approval

This study was approved by the Ethics Committee of the Sun Yat-sen Memorial Hospital, Sun Yat-sen University (No. SYSEC-KY-KS-2021–005).

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 28 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Han, Q., Liang, P., Li, J. et al. The ratio of neutrophil to lymphocyte as a potential marker of clinicopathological activity for lupus nephritis. Int Urol Nephrol 56, 675–682 (2024). https://doi.org/10.1007/s11255-023-03704-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11255-023-03704-z

Keywords

Search

Navigation