- Original article
- Open Access
Correlation of serum interleukin-10 level with disease activity and severity in systemic lupus erythematosus
Egyptian Rheumatology and Rehabilitation volume 45, pages 25–33 (2018)
Systemic lupus erythematosus (SLE, lupus) is a syndrome of multifactorial etiology, characterized by widespread inflammation, most commonly affecting women during the childbearing years. Virtually, every organ and/or system of the body may be involved. Interleukin-10 (IL-10) production is increased in SLE.
The aim of the study was to assess serum levels of IL-10 in SLE patients and their relationship with disease activity and severity parameters.
Patients and methods
Totally, 50 patients with SLE and 20 healthy controls were investigated in this study diagnosed according to Systemic Lupus International Collaborating Clinics (SLICC) classification criteria for SLE. Clinical assessment of the disease activity was performed using the Systemic Lupus Erythematosus Disease Activity Index (SLEDAI) score. Assessment of SLE disease severity was carried out using the SLICC/American College of Rheumatology Damage Index and laboratory parameters, including erythrocyte sedimentation rate, C-reactive protein (CRP), 24 h urinary proteins, anti-dsDNA antibodies, complement 3, and complement 4 levels. The serum IL-10 levels were determined using enzyme-linked immune sorbent assay technique.
The serum IL-10 levelswere significantly higher in SLE patients (mean: 23.07±33.19 pg/ ml) compared with the controls (0.52±0.86 pg/ml, P=0.000*). The increase in serum levels IL-10 significantly correlated with the SLEDAI scores (P=0.016*) and CRP (P=0.042*) in the studied patients. There were no significant correlations between IL-10 and SLICC, age, disease duration, erythrocyte sedimentation rate, 24 h urinary protein, anti-DNA, and complement 3–complement 4 (P=0.735; r=0.05, P=0.890, P=0.521, P=0.529; r=0.09, P=0.430; r=0.11, P=0.263; r=0.16, P=0.195; r=0.19, respectively).
There was no significant difference between mean IL-10 levels in different classes of lupus nephritis (P=0.702).
The circulating IL-10 concentrations were significantly elevated in SLE patients and correlated with the SLEDAI score and CRP.
Peng H, Wang W, Zhou M, Li R, Pan HF, Ye DQ. Role of interleukin-10 and interleukin-10 receptor in systemic lupus erythematosus. Clin Rheumatol 2013; 32:1255–1266.
Lorente L, Richaud PY, Wijdenes J, Alcocer-Varela J, Maillot MC, et al. Spontaneous production of interleukin-10 by B lymphocytes and monocytes in systemic lupus erythematosus. Eur Cytokine Netw 1993; 4:421–427.
Shalev I, Schmelzle M, Robson SC, Levy G. Making sense of regulatory T cell suppressive function. Semin Immunol 2011; 23:282–292.
Yin Z, Bahtiyar G, Zhang N, Liu L, Zhu P, et al. IL-10 regulates murine lupus. J Immunol 2002; 169:2148–2155.
Yin Z, Huang J, He W, Cao Z, Luo X, Zhang C. Serum level of eight cytokines in Han Chinese patients with systemic lupus erythematosus using multiplex fluorescent microsphere method. Centr Eur J Immunol 2014; 39:228–235.
Da Silva HD, da Silva AP, da Silva HA, Asano NM, Maia Mde M, de Souza PR. Interferon gamma and interleukin 10 polymorphisms in Brazilian patients with systemic lupus erythematosus. Mol Biol Rep 2014; 41:2493–2500.
Petri M, Orbai AM, Alarcón GS, Gordon C, Merrill JT, Fortin PR. Derivation and validation of Systemic Lupus International Collaborating Clinics Classification Criteria for Systemic Lupus Erythematosus. Arthritis Rheum 2012; 64:2677–2686.
Gladman DD, Ibañez D, Urowitz MB. Systemic lupus erythematosus disease activity index 2000. J Rheumatol 2002; 29:288–291.
Newland J, Goldman L, Ausiello D. The peripheral blood smear. In: Wyngaarden JB, Smith LH Jr, Claude Bennett J, editors. Cecil medicine. 23rd ed. Philadelphia, PA, USA: Saunders Elsevier; 2007. 161:1212–1216.
Dacie V, Lewis M. Practicle heamatology Vol. 12. 6th ed. Edinburgh, London: Churchil Livingstone; 1984. 4220.
Karlson D, Elizabeth W, Paul M, Ridker M, Maher N, JoAnn E, Manson M. C-reactive protein in the prediction of rheumatoid arthritis in women. Arch Intern Med 2006; 166:2490–2494.
De Bruijn MH, Fey GH. Human complement component C3: cDNA coding sequence and derived primary structure. Proc Natl Acad Sci USA 1985; 82:708–712.
Aitcheston C, Tan C. Antinuclear antibody in scientific basis of rheumatology. In: Panayi GS (editor). Edinburgh, London, Melbourne and New York: Churil Livingstone; 1982. 87.
Okamura M, Kanayama Y, Amastu K, Negoro N, Kohda S, Takeda T, et al. Significance of enzyme linked immune-sorbent assay (ELISA) for antibodies to double stranded and single stranded DNA in patients with lupus nephritis: correlation with severity of renal histology. Ann Rheum Dis 1993; 52:14–20.
Bazari H. Approach to the patient with renal disease. In: Goldman L, Ausiello D, editors. Cecil medicine. 23rd ed. Philadelphia, PA, USA: Saunders Elsevier; 2007. 115.
Weening JJ, D’Agati VD, Schwartz MM, Seshan SV, Alpers CE, Appel GB. The classification of glomerulonephritis in systemic lupus erythematosus revisited. Kidney Int 2004; 65:521–530.
Mok CC, Yap DY, Navarra SV, Liu ZH, Zhao MH, Lu L. Asian Lupus Nephritis Network (ALNN). Overview of lupus nephritis management guidelines and perspective from Asia. Nephrology (Carlton) 2014; 19:11–20.
Tiffin N, Adeyemo A, Okpechi I.A diverse array of genetic factors contribute to the pathogenesis of systemic lupus erythematosus. Orphanet J Rare Dis 2013; 8:2.
Rönnelid J, Tejde A, Mathsson L, Nilsson-Ekdahl K, Nilsson B. Immune complexes from SLE sera induce IL10 production from normal peripheral blood mononu clearcells by an FcgRII dependent mechanism: implications for a possible vicious cycle maintaining B cell hyperactivity in SLE. Ann Rheum Dis 2003; 62:37–42.
Tsokos GC. Mechanisms of diseases, systemic lupus erythematosus. N Engl J Med 2011; 365:2110–2121.
Hondowicz BD, Alexander ST, Quinn WJ, Pagán AJ, Metzgar MH, Cancro MP. The role of BLyS/BLyS receptors in anti-chromatin B cell regulation. Int Immunol 2007; 19:465–475.
Moulin V, Andris F, Thielemans K, Maliszewski C, Urbain J, Moser M. B lymphocytes regulate dendritic cell (DC) function in vivo: increased interleukin 12 production by DCs from B cell-deficient mice results in T helper cell type 1 deviation. J Exp Med 2000; 192:475–482.
Jacobi AM, Odendahl M, Reiter K, Bruns A, Burmester GR, et al. Correlation between circulating CD27 high plasma cells and disease activity in patients with systemic lupus erythematosus. Arthritis Rheum 2003; 48:1332–1342.
Sahar AF, Reem HA, Hanan S, Mohmad A. Serum interleukin-18 and interleukin-10 levels in systemic lupus erythematosus: correlation with SLEDAI score and disease activity parameters. Egypt Rheumatol Rehabil 2014; 41:160–166.
Liviu G, Vakkalanka RK, Elkon KB, Crow MK. Interleukin-10 promotes activation-induced cell death of SLE lymphocytes mediated by Fas Ligand. J Clin Invest 1997; 100:2622–2633.
Yin Z, Huang J, He W, Cao Z, Luo X, Zhang C. Serum level of eight cytokines in Han Chinese patients with systemic lupus erythematosus using multiplex fluorescent microsphere. Centr Eur J Immunol 2014; 39:228–235.
Yang X, Sun B, Wang H, Yin C, Wang X, et al. Increased serum IL-10 in lupus patients promotes apoptosis of T cell subsets via the caspase 8 pathway initiated by Fas signaling. J Biomed Res 2015; 29:232–240.
Ahmad AE, Kamal FM, Nisreen EE, Mai HR. Effects of interleukin-10 gene polymorphism on clinical diversity and activity of systemic lupus erythematosus. Egypt Rheumatol Rehabil 2015; 42:49–54.
Dhir V, Singh AP, Aggarwal A, Naik S, Misra R. Increased T-lymphocyte apoptosis in lupus correlates with disease activity and may be responsible for reduced T-cell frequency: a cross-sectional and longitudinal study. Lupus 2009; 18:785–791.
Chen J, Shen B, Jiang Y, Jun L, Zhu M, Chen B. Analysis of immunoglobulin-like transcripts (ILTs) in lymphocytes with sHLA-G and IL10 from SLE patients. Clin Exp Med 2013; 13:135–142.
Ishida H, Muchamuel T, Sakaguchi S, Andrade S, Menon S, Howard M. Continuous administration of anti-interleukin 10 antibodies delays onset of autoimmunity in NZB/W F1 mice. J Exp Med 1994; 179:305–310.
Park YB, Lee SK, Kim DS, Lee J, Lee CH, Song CH. Elevated interleukin-10 levels correlated with disease activity in systemic lupus erythematosus. Clin Exp Rheumatol 1998; 16:283–288.
Chun HY, Chung JW, Kim HA, Yun JM, Jeon JY, Ye YM. Cytokine IL-6 and IL-10 as biomarkers in systemic lupus erythematosus. J Clin Immunol 2007; 27:461–466.
Koenig KF, Groeschi I, Pesickova SS, Tesar V, Eisenberger U, Trendelenburg M. Serum cytokine profile in patients with active lupus nephritis. Cytokine 2012; 60:410–416.
Lorente L, Richaud PY, Garcia PC, Claret E, Jakez OJ, et al. Clinical and biologic effects of anti-interleukin-10 monoclonal antibody administration in systemic lupus erythematosus. Arthritis Rheum 2000; 43:1790–1800.
Arora V, Verma J, Marwah V, Kumar A, Anand D, Das N. Cytokine imbalance in systemic lupus erythematosus: a study on northern Indian subjects. Lupus 2012; 21:596–603.
Lacki JK, Samborski W, Mackiewicz SH. Interleukin-10 and interleukin-6 in lupus erythematosus and rheumatoid arthritis, correlations with acute phase proteins. Clin Rheumatol 1997; 16:275–278.
Capper ER, Maskill JK, Gordon C, Blakemore A IF. Interleukin (IL)-10, IL-1ra and IL-12 profiles in active and quiescent systemic lupus erythematosus: could longitudinal studies reveal patient subgroups of differing pathology. Clin Exp Immunol 2004; 138:348–356.
Sikka G, Miller KL, Steppan J, Pandey D, Jung SM, Fraser CD. Interleukin 10 knockout frail mice develop cardiac and vascular dysfunction with increased age. Exp Gerontol 2013; 48:128–135.
Sameh AZ, Ghada K, Malak N. IL10 in lupus nephritis: detection and relationship with disease activity. Electron Physician 2015; 7: 1680–1685.
Houssiau FA, Lefebvre C, Vanden Berghe M, Lambert M, Devogelaer JP, Renauld JC. Serum interleukin 10 titers in systemic lupus erythematosus reflect disease activity. Lupus 1995; 4:393–395.
El-Sayed M, Nofal E, Al Mokadem S, Al Makhzangy I, Gaballah H, Hossneia A. Correlative study of serum Th1/Th2 cytokines levels in patients with systemic lupus erythematosus with SLEDAI. Egypt Dermatol Online J 2008; 4:3.
Ma L, Zhao P, Jiang Z, Shan Y, Jiang Y. Imbalance of different types of CD4 +forkhead box protein 3 (FoxP3)+ T cells in patients with new-onset systemic lupus erythematosus. Clin Exp Immunol 2013; 174:345–355.
Eoghan MM, Siobha N, Ruth ZL, Gaye C, Michele F, Donnelly S. The association of cytokines with disease activity and damage scores in systemic lupus erythematosus patients. Rheumatology (Oxford) 2014; 53:1586–1594.
Ravirajan CT, Wang Y, Matis LA, Papadaki L, Griffiths MH, Latchman DS. Effect of neutralizing antibodies to IL-10 and C5 on the renal damage caused by a pathogenic human anti-dsDNA antibody. Rheumatology (Oxford) 2004; 43:442–447.
This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 3.0 License, which allows others to remix, tweak, and build upon the work noncommercially, as long as the author is credited and the new creations are licensed under the identical terms.
About this article
Cite this article
Abd Elazeem, M.I., Mohammed, R.A. & Abdallah, N.H. Correlation of serum interleukin-10 level with disease activity and severity in systemic lupus erythematosus. Egypt Rheumatol Rehabil 45, 25–33 (2018). https://doi.org/10.4103/err.err_15_17
- enzyme-linked immune sorbent assay
- systemic lupus erythematosus
- systemic lupus erythematosus disease activity index