Skip to main content
Top
Published in: Pediatric Nephrology 9/2017

01-09-2017 | Original Article

Anti-C1q autoantibodies as markers of renal involvement in childhood-onset systemic lupus erythematosus

Authors: Cécile Picard, Jean-Christophe Lega, Bruno Ranchin, Pierre Cochat, Natalia Cabrera, Nicole Fabien, Alexandre Belot

Published in: Pediatric Nephrology | Issue 9/2017

Login to get access

Abstract

Background

Childhood-onset systemic lupus erythematosus (cSLE) is rare, and considered more severe than its adult-onset counterpart. Lupus nephritis (LN) occurs more frequently in children, accounting for higher long-term morbidity and mortality compared with adults. Thus, reliable biological markers are needed to predict disease course. This study aimed to investigate the capacity of anti-C1q autoantibodies (Abs) to predict renal flare and global disease activity in cSLE patients, and association with disease activity and kidney involvement.

Methods

Twenty-eight patients with cSLE including 19 patients (68%) with a history of LN were included retrospectively. Anti-C1q Abs were analysed by ELISA at renal flare-up or in the quiescent phase of disease and compared with Farr dsDNA assay.

Results

Thirty-one flares occurred during follow-up: anti-C1q Abs were positive in 26 (84%), strongly associated with active disease status (p < 0.0001), and correlated with global disease activity score (p < 0.0001) and anti-dsDNA Abs presence (p < 0.0001). The specificity of anti-C1q Abs was higher than anti-dsDNA (73% vs 19%) in discriminating LN patients, whereas the receiver operating characteristic curves were not statistically different (0.83 ± 0.06 vs 0.78 ± 0.08 respectively), similar to C3 dosage. The presence of anti-C1q Abs at diagnosis was not predictive for global or renal flare. Introduction of a modified SLEDAI score excluding dsDNA Abs, demonstrated a stronger correlation of anti-C1q Abs titres with SLEDAI score in comparison with the Farr test.

Conclusion

Anti-C1q Abs seem very specific to flares, including LN in children, and their role in daily practice compared with the Farr dsDNA assay needs to be defined.
Appendix
Available only for authorised users
Literature
2.
go back to reference Ramos PS, Kelly JA, Gray-McGuire C, Bruner GR, Leiran AN, Meyer CM, Namjou B, Espe KJ, Ortmann WA, Reichlin M, Langefeld CD, James JA, Gaffney PM, Behrens TW, Harley JB, Moser KL (2006) Familial aggregation and linkage analysis of autoantibody traits in pedigrees multiplex for systemic lupus erythematosus. Genes Immun 7:417–432CrossRefPubMed Ramos PS, Kelly JA, Gray-McGuire C, Bruner GR, Leiran AN, Meyer CM, Namjou B, Espe KJ, Ortmann WA, Reichlin M, Langefeld CD, James JA, Gaffney PM, Behrens TW, Harley JB, Moser KL (2006) Familial aggregation and linkage analysis of autoantibody traits in pedigrees multiplex for systemic lupus erythematosus. Genes Immun 7:417–432CrossRefPubMed
3.
go back to reference Webb R, Kelly JA, Somers EC, Hughes T, Kaufman KM, Sanchez E, Nath SK, Bruner G, Alarcón-Riquelme ME, Gilkeson GS, Kamen DL, Richardson BC, Harley JB, Sawalha AH (2011) Early disease onset is predicted by a higher genetic risk for lupus and is associated with a more severe phenotype in lupus patients. Ann Rheum Dis 70:151–156CrossRefPubMed Webb R, Kelly JA, Somers EC, Hughes T, Kaufman KM, Sanchez E, Nath SK, Bruner G, Alarcón-Riquelme ME, Gilkeson GS, Kamen DL, Richardson BC, Harley JB, Sawalha AH (2011) Early disease onset is predicted by a higher genetic risk for lupus and is associated with a more severe phenotype in lupus patients. Ann Rheum Dis 70:151–156CrossRefPubMed
4.
5.
go back to reference Brunner HI, Gladman DD, Ibañez D, Urowitz MD, Silverman ED (2008) Difference in disease features between childhood-onset and adult-onset systemic lupus erythematosus. Arthritis Rheum 58:556–562CrossRefPubMed Brunner HI, Gladman DD, Ibañez D, Urowitz MD, Silverman ED (2008) Difference in disease features between childhood-onset and adult-onset systemic lupus erythematosus. Arthritis Rheum 58:556–562CrossRefPubMed
7.
go back to reference Agnello V, Koffler D, Eisenberg JW, Winchester RJ, Kundel HG (1971) C1g precipitins in the sera of patients with systemic lupus erythematosus and other hypocomplementemic states: characterization of high and low molecular weight types. J Exp Med 134:228s–241sPubMed Agnello V, Koffler D, Eisenberg JW, Winchester RJ, Kundel HG (1971) C1g precipitins in the sera of patients with systemic lupus erythematosus and other hypocomplementemic states: characterization of high and low molecular weight types. J Exp Med 134:228s–241sPubMed
8.
go back to reference Pickering MC, Botto M (2010) Are anti-C1q antibodies different from other SLE autoantibodies? Nat Rev Rheumatol 6:490–493CrossRefPubMed Pickering MC, Botto M (2010) Are anti-C1q antibodies different from other SLE autoantibodies? Nat Rev Rheumatol 6:490–493CrossRefPubMed
9.
go back to reference Mohan C, Putterman C (2015) Genetics and pathogenesis of systemic lupus erythematosus and lupus nephritis. Nat Rev Nephrol 11:329–341CrossRefPubMed Mohan C, Putterman C (2015) Genetics and pathogenesis of systemic lupus erythematosus and lupus nephritis. Nat Rev Nephrol 11:329–341CrossRefPubMed
10.
go back to reference Lood C, Gullstrand B, Truedsson L, Olin AI, Alm GV, Rönnblom L, Sturfelt G, Eloranta M-L, Bengtsson AA (2009) C1q inhibits immune complex-induced interferon-alpha production in plasmacytoid dendritic cells: a novel link between C1q deficiency and systemic lupus erythematosus pathogenesis. Arthritis Rheum 60:3081–3090CrossRefPubMed Lood C, Gullstrand B, Truedsson L, Olin AI, Alm GV, Rönnblom L, Sturfelt G, Eloranta M-L, Bengtsson AA (2009) C1q inhibits immune complex-induced interferon-alpha production in plasmacytoid dendritic cells: a novel link between C1q deficiency and systemic lupus erythematosus pathogenesis. Arthritis Rheum 60:3081–3090CrossRefPubMed
11.
go back to reference Schaller M, Bigler C, Danner D, Ditzel HJ, Trendelenburg M (2009) Autoantibodies against C1q in systemic lupus erythematosus are antigen-driven. J Immunol 183:8225–8231CrossRefPubMed Schaller M, Bigler C, Danner D, Ditzel HJ, Trendelenburg M (2009) Autoantibodies against C1q in systemic lupus erythematosus are antigen-driven. J Immunol 183:8225–8231CrossRefPubMed
12.
go back to reference Fatemi A, Samadi G, Sayedbonakdar Z, Smiley A (2016) Anti-C1q antibody in patients with lupus nephritic flare: 18-month follow-up and a nested case–control study. Mod Rheumatol 26:233–239CrossRefPubMed Fatemi A, Samadi G, Sayedbonakdar Z, Smiley A (2016) Anti-C1q antibody in patients with lupus nephritic flare: 18-month follow-up and a nested case–control study. Mod Rheumatol 26:233–239CrossRefPubMed
13.
go back to reference Leffler J, Bengtsson AA, Blom AM (2014) The complement system in systemic lupus erythematosus: an update. Ann Rheum Dis 73:1601–1606CrossRefPubMed Leffler J, Bengtsson AA, Blom AM (2014) The complement system in systemic lupus erythematosus: an update. Ann Rheum Dis 73:1601–1606CrossRefPubMed
14.
go back to reference Chen Z, Wang G-S, Wang G-H, Li X-P (2012) Anti-C1q antibody is a valuable biological marker for prediction of renal pathological characteristics in lupus nephritis. Clin Rheumatol 31:1323–1329CrossRefPubMed Chen Z, Wang G-S, Wang G-H, Li X-P (2012) Anti-C1q antibody is a valuable biological marker for prediction of renal pathological characteristics in lupus nephritis. Clin Rheumatol 31:1323–1329CrossRefPubMed
15.
go back to reference Akhter E, Burlingame RW, Seaman AL, Magder L, Petri M (2011) Anti-C1q antibodies have higher correlation with flares of lupus nephritis than other serum markers. Lupus 20:1267–1274CrossRefPubMed Akhter E, Burlingame RW, Seaman AL, Magder L, Petri M (2011) Anti-C1q antibodies have higher correlation with flares of lupus nephritis than other serum markers. Lupus 20:1267–1274CrossRefPubMed
16.
go back to reference Matrat A, Veysseyre-Balter C, Trolliet P, Villar E, Dijoud F, Bienvenu J, Fabien N (2011) Simultaneous detection of anti-C1q and anti-double stranded DNA autoantibodies in lupus nephritis: predictive value for renal flares. Lupus 20:28–34CrossRefPubMed Matrat A, Veysseyre-Balter C, Trolliet P, Villar E, Dijoud F, Bienvenu J, Fabien N (2011) Simultaneous detection of anti-C1q and anti-double stranded DNA autoantibodies in lupus nephritis: predictive value for renal flares. Lupus 20:28–34CrossRefPubMed
17.
go back to reference Orbai A-M, Truedsson L, Sturfelt G, Nived O, Fang H, Alarcón GS, Gordon C, Merrill J, Fortin PR, Bruce IN, Isenberg DA, Wallace DJ, Ramsey-Goldman R, Bae S-C, Hanly JG, Sanchez-Guerrero J, Clarke AE, Aranow CB, Manzi S, Urowitz MB, Gladman DD, Kalunian KC, Costner MI, Werth VP, Zoma A, Bernatsky S, Ruiz-Irastorza G, Khamashta MA, Jacobsen S, Buyon JP, Maddison P, Dooley MA, Van Vollenhoven RF, Ginzler E, Stoll T, Peschken C, Jorizzo JL, Callen JP, Lim SS, Fessler BJ, Inanc M, Kamen DL, Rahman A, Steinsson K, Franks AG, Sigler L, Hameed S, Pham N, Brey R, Weisman MH, McGwin G, Magder LS, Petri M (2015) Anti-C1q antibodies in systemic lupus erythematosus. Lupus 24:42–49CrossRefPubMed Orbai A-M, Truedsson L, Sturfelt G, Nived O, Fang H, Alarcón GS, Gordon C, Merrill J, Fortin PR, Bruce IN, Isenberg DA, Wallace DJ, Ramsey-Goldman R, Bae S-C, Hanly JG, Sanchez-Guerrero J, Clarke AE, Aranow CB, Manzi S, Urowitz MB, Gladman DD, Kalunian KC, Costner MI, Werth VP, Zoma A, Bernatsky S, Ruiz-Irastorza G, Khamashta MA, Jacobsen S, Buyon JP, Maddison P, Dooley MA, Van Vollenhoven RF, Ginzler E, Stoll T, Peschken C, Jorizzo JL, Callen JP, Lim SS, Fessler BJ, Inanc M, Kamen DL, Rahman A, Steinsson K, Franks AG, Sigler L, Hameed S, Pham N, Brey R, Weisman MH, McGwin G, Magder LS, Petri M (2015) Anti-C1q antibodies in systemic lupus erythematosus. Lupus 24:42–49CrossRefPubMed
18.
go back to reference Sinico RA, Rimoldi L, Radice A, Bianchi L, Gallelli B, Moroni G (2009) Anti-C1q autoantibodies in lupus nephritis. Ann N Y Acad Sci 1173:47–51CrossRefPubMed Sinico RA, Rimoldi L, Radice A, Bianchi L, Gallelli B, Moroni G (2009) Anti-C1q autoantibodies in lupus nephritis. Ann N Y Acad Sci 1173:47–51CrossRefPubMed
19.
go back to reference Moroni G, Radice A, Giammarresi G, Quaglini S, Gallelli B, Leoni A, Li Vecchi M, Vecchi ML, Messa P, Sinico RA (2009) Are laboratory tests useful for monitoring the activity of lupus nephritis? A 6-year prospective study in a cohort of 228 patients with lupus nephritis. Ann Rheum Dis 68:234–237CrossRefPubMed Moroni G, Radice A, Giammarresi G, Quaglini S, Gallelli B, Leoni A, Li Vecchi M, Vecchi ML, Messa P, Sinico RA (2009) Are laboratory tests useful for monitoring the activity of lupus nephritis? A 6-year prospective study in a cohort of 228 patients with lupus nephritis. Ann Rheum Dis 68:234–237CrossRefPubMed
20.
go back to reference Gilliam BE, Ombrello AK, Burlingame RW, Pepmueller PH, Moore TL (2012) Measurement of autoantibodies in pediatric-onset systemic lupus erythematosus and their relationship with disease-associated manifestations. Semin Arthritis Rheum 41:840–848CrossRefPubMed Gilliam BE, Ombrello AK, Burlingame RW, Pepmueller PH, Moore TL (2012) Measurement of autoantibodies in pediatric-onset systemic lupus erythematosus and their relationship with disease-associated manifestations. Semin Arthritis Rheum 41:840–848CrossRefPubMed
21.
go back to reference Kozyro I, Perahud I, Sadallah S, Sukalo A, Titov L, Schifferli J, Trendelenburg M (2006) Clinical value of autoantibodies against C1q in children with glomerulonephritis. Pediatrics 117:1663–1668CrossRefPubMed Kozyro I, Perahud I, Sadallah S, Sukalo A, Titov L, Schifferli J, Trendelenburg M (2006) Clinical value of autoantibodies against C1q in children with glomerulonephritis. Pediatrics 117:1663–1668CrossRefPubMed
22.
go back to reference Cervera R, Khamashta MA, Font J, Sebastiani GD, Gil A, Lavilla P, Doménech I, Aydintug AO, Jedryka-Góral A, de Ramón E (1993) Systemic lupus erythematosus: clinical and immunologic patterns of disease expression in a cohort of 1,000 patients. The European Working Party on Systemic Lupus Erythematosus. Medicine (Baltimore) 72:113–124CrossRef Cervera R, Khamashta MA, Font J, Sebastiani GD, Gil A, Lavilla P, Doménech I, Aydintug AO, Jedryka-Góral A, de Ramón E (1993) Systemic lupus erythematosus: clinical and immunologic patterns of disease expression in a cohort of 1,000 patients. The European Working Party on Systemic Lupus Erythematosus. Medicine (Baltimore) 72:113–124CrossRef
23.
go back to reference Pande I, Sekharan NG, Kailash S, Uppal SS, Singh RR, Kumar A, Malaviya AN (1993) Analysis of clinical and laboratory profile in Indian childhood systemic lupus erythematosus and its comparison with SLE in adults. Lupus 2:83–87CrossRefPubMed Pande I, Sekharan NG, Kailash S, Uppal SS, Singh RR, Kumar A, Malaviya AN (1993) Analysis of clinical and laboratory profile in Indian childhood systemic lupus erythematosus and its comparison with SLE in adults. Lupus 2:83–87CrossRefPubMed
24.
go back to reference Carreño L, López-Longo FJ, Monteagudo I, Rodríguez-Mahou M, Bascones M, González CM, Saint-Cyr C, Lapointe N (1999) Immunological and clinical differences between juvenile and adult onset of systemic lupus erythematosus. Lupus 8:287–292CrossRefPubMed Carreño L, López-Longo FJ, Monteagudo I, Rodríguez-Mahou M, Bascones M, González CM, Saint-Cyr C, Lapointe N (1999) Immunological and clinical differences between juvenile and adult onset of systemic lupus erythematosus. Lupus 8:287–292CrossRefPubMed
25.
go back to reference Barron KS, Silverman ED, Gonzales J, Reveille JD (1993) Clinical, serologic, and immunogenetic studies in childhood-onset systemic lupus erythematosus. Arthritis Rheum 36:348–354CrossRefPubMed Barron KS, Silverman ED, Gonzales J, Reveille JD (1993) Clinical, serologic, and immunogenetic studies in childhood-onset systemic lupus erythematosus. Arthritis Rheum 36:348–354CrossRefPubMed
26.
go back to reference Amaral B, Murphy G, Ioannou Y, Isenberg DA (2014) A comparison of the outcome of adolescent and adult-onset systemic lupus erythematosus. Rheumatology (Oxford) 53:1130–1135CrossRef Amaral B, Murphy G, Ioannou Y, Isenberg DA (2014) A comparison of the outcome of adolescent and adult-onset systemic lupus erythematosus. Rheumatology (Oxford) 53:1130–1135CrossRef
27.
go back to reference Hoffman IEA, Lauwerys BR, De Keyser F, Huizinga TWJ, Isenberg D, Cebecauer L, Dehoorne J, Joos R, Hendrickx G, Houssiau F, Elewaut D (2009) Juvenile-onset systemic lupus erythematosus: different clinical and serological pattern than adult-onset systemic lupus erythematosus. Ann Rheum Dis 68:412–415CrossRefPubMed Hoffman IEA, Lauwerys BR, De Keyser F, Huizinga TWJ, Isenberg D, Cebecauer L, Dehoorne J, Joos R, Hendrickx G, Houssiau F, Elewaut D (2009) Juvenile-onset systemic lupus erythematosus: different clinical and serological pattern than adult-onset systemic lupus erythematosus. Ann Rheum Dis 68:412–415CrossRefPubMed
28.
go back to reference Tucker LB, Uribe AG, Fernández M, Vilá LM, McGwin G, Apte M, Fessler BJ, Bastian HM, Reveille JD, Alarcón GS (2008) Adolescent onset of lupus results in more aggressive disease and worse outcomes: results of a nested matched case–control study within LUMINA, a multiethnic US cohort (LUMINA LVII). Lupus 17:314–322CrossRefPubMedPubMedCentral Tucker LB, Uribe AG, Fernández M, Vilá LM, McGwin G, Apte M, Fessler BJ, Bastian HM, Reveille JD, Alarcón GS (2008) Adolescent onset of lupus results in more aggressive disease and worse outcomes: results of a nested matched case–control study within LUMINA, a multiethnic US cohort (LUMINA LVII). Lupus 17:314–322CrossRefPubMedPubMedCentral
29.
go back to reference Hersh AO, von Scheven E, Yazdany J, Panopalis P, Trupin L, Julian L, Katz P, Criswell LA, Yelin E (2009) Differences in long-term disease activity and treatment of adult patients with childhood- and adult-onset systemic lupus erythematosus. Arthritis Rheum 61:13–20CrossRefPubMedPubMedCentral Hersh AO, von Scheven E, Yazdany J, Panopalis P, Trupin L, Julian L, Katz P, Criswell LA, Yelin E (2009) Differences in long-term disease activity and treatment of adult patients with childhood- and adult-onset systemic lupus erythematosus. Arthritis Rheum 61:13–20CrossRefPubMedPubMedCentral
30.
go back to reference Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH, Austin A, Bell A, Bloch DA, Corey PN, Decker JL, Esdaile J, Fries JF, Ginzler EM, Goldsmith CH, Hochberg MC, Jones JV, Riche NGHL, Liang MH, Lockshin MD, Muenz LR, Sackett DL, Schur PH (1992) Derivation of the SLEDAI. A disease activity index for lupus patients. Arthritis Rheum 35:630–640CrossRefPubMed Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH, Austin A, Bell A, Bloch DA, Corey PN, Decker JL, Esdaile J, Fries JF, Ginzler EM, Goldsmith CH, Hochberg MC, Jones JV, Riche NGHL, Liang MH, Lockshin MD, Muenz LR, Sackett DL, Schur PH (1992) Derivation of the SLEDAI. A disease activity index for lupus patients. Arthritis Rheum 35:630–640CrossRefPubMed
31.
go back to reference Beurskens FJ, van Schaarenburg RA, Trouw LA (2015) C1q, antibodies and anti-C1q autoantibodies. Mol Immunol 68:6–13CrossRefPubMed Beurskens FJ, van Schaarenburg RA, Trouw LA (2015) C1q, antibodies and anti-C1q autoantibodies. Mol Immunol 68:6–13CrossRefPubMed
33.
go back to reference Jesus AA, Silva CA, Carneiro-Sampaio M, Sheinberg M, Mangueira CL, Marie SK, Liphaus BL (2009) Anti-C1q antibodies in juvenile-onset systemic lupus erythematosus. Ann N Y Acad Sci 1173:235–238CrossRefPubMed Jesus AA, Silva CA, Carneiro-Sampaio M, Sheinberg M, Mangueira CL, Marie SK, Liphaus BL (2009) Anti-C1q antibodies in juvenile-onset systemic lupus erythematosus. Ann N Y Acad Sci 1173:235–238CrossRefPubMed
34.
go back to reference Wu FQ, Zhao Q, Cui XD, Zhang W (2011) C1q and anti-C1q antibody levels are correlated with disease severity in Chinese pediatric systemic lupus erythematosus. Rheumatol Int 31:501–505CrossRefPubMed Wu FQ, Zhao Q, Cui XD, Zhang W (2011) C1q and anti-C1q antibody levels are correlated with disease severity in Chinese pediatric systemic lupus erythematosus. Rheumatol Int 31:501–505CrossRefPubMed
35.
go back to reference Kamphuis S, Silverman ED (2010) Prevalence and burden of pediatric-onset systemic lupus erythematosus. Nat Rev Rheumatol 6:538–546CrossRefPubMed Kamphuis S, Silverman ED (2010) Prevalence and burden of pediatric-onset systemic lupus erythematosus. Nat Rev Rheumatol 6:538–546CrossRefPubMed
36.
go back to reference Marto N, Bertolaccini ML, Calabuig E, Hughes GRV, Khamashta MA (2005) Anti-C1q antibodies in nephritis: correlation between titres and renal disease activity and positive predictive value in systemic lupus erythematosus. Ann Rheum Dis 64:444–448CrossRefPubMed Marto N, Bertolaccini ML, Calabuig E, Hughes GRV, Khamashta MA (2005) Anti-C1q antibodies in nephritis: correlation between titres and renal disease activity and positive predictive value in systemic lupus erythematosus. Ann Rheum Dis 64:444–448CrossRefPubMed
37.
go back to reference Moroni G, Trendelenburg M, Del Papa N, Quaglini S, Raschi E, Panzeri P, Testoni C, Tincani A, Banfi G, Balestrieri G, Schifferli JA, Meroni PL, Ponticelli C (2001) Anti-C1q antibodies may help in diagnosing a renal flare in lupus nephritis. Am J Kidney Dis 37:490–498CrossRefPubMed Moroni G, Trendelenburg M, Del Papa N, Quaglini S, Raschi E, Panzeri P, Testoni C, Tincani A, Banfi G, Balestrieri G, Schifferli JA, Meroni PL, Ponticelli C (2001) Anti-C1q antibodies may help in diagnosing a renal flare in lupus nephritis. Am J Kidney Dis 37:490–498CrossRefPubMed
38.
go back to reference Katsumata Y, Miyake K, Kawaguchi Y, Okamoto Y, Kawamoto M, Gono T, Baba S, Hara M, Yamanaka H (2011) Anti-C1q antibodies are associated with systemic lupus erythematosus global activity but not specifically with nephritis: a controlled study of 126 consecutive patients. Arthritis Rheum 63:2436–2444CrossRefPubMed Katsumata Y, Miyake K, Kawaguchi Y, Okamoto Y, Kawamoto M, Gono T, Baba S, Hara M, Yamanaka H (2011) Anti-C1q antibodies are associated with systemic lupus erythematosus global activity but not specifically with nephritis: a controlled study of 126 consecutive patients. Arthritis Rheum 63:2436–2444CrossRefPubMed
39.
go back to reference Eggleton P, Ukoumunne OC, Cottrell I, Khan A, Maqsood S, Thornes J, Perry E, Isenberg D (2014) Autoantibodies against C1q as a diagnostic measure of lupus nephritis: systematic review and meta-analysis. J Clin Cell Immunol 5:210PubMedPubMedCentral Eggleton P, Ukoumunne OC, Cottrell I, Khan A, Maqsood S, Thornes J, Perry E, Isenberg D (2014) Autoantibodies against C1q as a diagnostic measure of lupus nephritis: systematic review and meta-analysis. J Clin Cell Immunol 5:210PubMedPubMedCentral
40.
go back to reference Seelen MA, Trouw LA, Daha MR (2003) Diagnostic and prognostic significance of anti-C1q antibodies in systemic lupus erythematosus. Curr Opin Nephrol Hypertens 12:619–624CrossRefPubMed Seelen MA, Trouw LA, Daha MR (2003) Diagnostic and prognostic significance of anti-C1q antibodies in systemic lupus erythematosus. Curr Opin Nephrol Hypertens 12:619–624CrossRefPubMed
41.
go back to reference Cai X, Yang X, Lian F, Lin X, Liang M, Li J, Chen X, Liang L, Qin S, Fu J (2010) Correlation between serum anti-C1q antibody levels and renal pathological characteristics and prognostic significance of anti-C1q antibody in lupus nephritis. J Rheumatol 37:759–765CrossRefPubMed Cai X, Yang X, Lian F, Lin X, Liang M, Li J, Chen X, Liang L, Qin S, Fu J (2010) Correlation between serum anti-C1q antibody levels and renal pathological characteristics and prognostic significance of anti-C1q antibody in lupus nephritis. J Rheumatol 37:759–765CrossRefPubMed
42.
go back to reference Yang X, Tan Y, Yu F, Zhao M (2012) Combination of anti-C1q and anti-dsDNA antibodies is associated with higher renal disease activity and predicts renal prognosis of patients with lupus nephritis. Nephrol Dial Transplant 27:3552–3559CrossRefPubMed Yang X, Tan Y, Yu F, Zhao M (2012) Combination of anti-C1q and anti-dsDNA antibodies is associated with higher renal disease activity and predicts renal prognosis of patients with lupus nephritis. Nephrol Dial Transplant 27:3552–3559CrossRefPubMed
43.
go back to reference Horváth L, Czirják L, Fekete B, Jakab L, Pozsonyi T, Kalabay L, Romics L, Miklós K, Varga L, Prohászka Z, Szakács A, Nagy E, Daha MR, Füst G (2001) High levels of antibodies against Clq are associated with disease activity and nephritis but not with other organ manifestations in SLE patients. Clin Exp Rheumatol 19:667–672PubMed Horváth L, Czirják L, Fekete B, Jakab L, Pozsonyi T, Kalabay L, Romics L, Miklós K, Varga L, Prohászka Z, Szakács A, Nagy E, Daha MR, Füst G (2001) High levels of antibodies against Clq are associated with disease activity and nephritis but not with other organ manifestations in SLE patients. Clin Exp Rheumatol 19:667–672PubMed
44.
go back to reference Trouw LA, Groeneveld TWL, Seelen MA, Duijs JMGJ, Bajema IM, Prins FA, Kishore U, Salant DJ, Verbeek JS, van Kooten C, Daha MR (2004) Anti-C1q autoantibodies deposit in glomeruli but are only pathogenic in combination with glomerular C1q-containing immune complexes. J Clin Invest 114:679–688CrossRefPubMedPubMedCentral Trouw LA, Groeneveld TWL, Seelen MA, Duijs JMGJ, Bajema IM, Prins FA, Kishore U, Salant DJ, Verbeek JS, van Kooten C, Daha MR (2004) Anti-C1q autoantibodies deposit in glomeruli but are only pathogenic in combination with glomerular C1q-containing immune complexes. J Clin Invest 114:679–688CrossRefPubMedPubMedCentral
45.
go back to reference Bigler C, Schaller M, Perahud I, Osthoff M, Trendelenburg M (2009) Autoantibodies against complement C1q specifically target C1q bound on early apoptotic cells. J Immunol 183:3512–3521CrossRefPubMed Bigler C, Schaller M, Perahud I, Osthoff M, Trendelenburg M (2009) Autoantibodies against complement C1q specifically target C1q bound on early apoptotic cells. J Immunol 183:3512–3521CrossRefPubMed
46.
go back to reference Petri M, Genovese M, Engle E, Hochberg M (1991) Definition, incidence, and clinical description of flare in systemic lupus erythematosus. A prospective cohort study. Arthritis Rheum 34:937–944CrossRefPubMed Petri M, Genovese M, Engle E, Hochberg M (1991) Definition, incidence, and clinical description of flare in systemic lupus erythematosus. A prospective cohort study. Arthritis Rheum 34:937–944CrossRefPubMed
47.
go back to reference Esdaile JM, Abrahamowicz M, Joseph L, MacKenzie T, Li Y, Danoff D (1996) Laboratory tests as predictors of disease exacerbations in systemic lupus erythematosus. Why some tests fail. Arthritis Rheum 39:370–378CrossRefPubMed Esdaile JM, Abrahamowicz M, Joseph L, MacKenzie T, Li Y, Danoff D (1996) Laboratory tests as predictors of disease exacerbations in systemic lupus erythematosus. Why some tests fail. Arthritis Rheum 39:370–378CrossRefPubMed
48.
go back to reference Coppo R, Peruzzi L, Amore A, Martino S, Vergano L, Lastauka I, Schieppati A, Noris M, Tovo PA, Remuzzi G (2014) Dramatic effects of eculizumab in a child with diffuse proliferative lupus nephritis resistant to conventional therapy. Pediatr Nephrol 30:167–172CrossRefPubMed Coppo R, Peruzzi L, Amore A, Martino S, Vergano L, Lastauka I, Schieppati A, Noris M, Tovo PA, Remuzzi G (2014) Dramatic effects of eculizumab in a child with diffuse proliferative lupus nephritis resistant to conventional therapy. Pediatr Nephrol 30:167–172CrossRefPubMed
Metadata
Title
Anti-C1q autoantibodies as markers of renal involvement in childhood-onset systemic lupus erythematosus
Authors
Cécile Picard
Jean-Christophe Lega
Bruno Ranchin
Pierre Cochat
Natalia Cabrera
Nicole Fabien
Alexandre Belot
Publication date
01-09-2017
Publisher
Springer Berlin Heidelberg
Published in
Pediatric Nephrology / Issue 9/2017
Print ISSN: 0931-041X
Electronic ISSN: 1432-198X
DOI
https://doi.org/10.1007/s00467-017-3646-z

Other articles of this Issue 9/2017

Pediatric Nephrology 9/2017 Go to the issue