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Published in: Pediatric Nephrology 3/2013

01-03-2013 | Review

Urine biomarkers in juvenile-onset SLE nephritis

Authors: Louise Watson, Michael W. Beresford

Published in: Pediatric Nephrology | Issue 3/2013

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Abstract

Over 80 % of patients with juvenile-onset systemic lupus erythematosus will have renal involvement compared to 40 % with adult-onset disease. Up to 44 % of children who do have lupus nephritis (LN) progress to renal failure in early adulthood. Improved methods of detecting onset of LN would allow earlier treatment, which may prevent irreversible renal scarring and a decline in renal function. Current conventional markers of disease activity fail to adequately predict renal lupus flares and include proteinuria, complement levels, anti-double-stranded DNA antibodies and serum creatinine concentrations. Standardized histological classification is currently the gold standard for diagnosing and classifying LN, but its invasive nature limits routine use for monitoring, especially in a childhood population. Novel biomarkers need to be sensitive and specific—and preferably non-invasive and cost-effective. The most promising biomarkers in juvenile-onset LN include urinary neutrophil gelatinase associated lipocalin, monocyte chemoattractant protein 1 and transforming growth factor-beta, although many others have been identified and are under investigation. No one biomarker yet discovered is unique to LN, indicating an overlap in disease pathophysiology. It is likely that a combination of biomarkers will be required for assessing disease flare detection, response to treatment and prognostic information. Potential biomarkers require longitudinal validation in large paediatric, prospective cohorts to assess their ability to act as clinically useful adjuncts.
Literature
1.
go back to reference Midgley A, Beresford MW (2011) Cellular localization of nuclear antigen during neutrophil apoptosis: mechanism for autoantigen exposure? Lupus 20:641–646PubMedCrossRef Midgley A, Beresford MW (2011) Cellular localization of nuclear antigen during neutrophil apoptosis: mechanism for autoantigen exposure? Lupus 20:641–646PubMedCrossRef
2.
go back to reference Tucker LB, Menon S, Schaller JG, Isenberg DA (1995) Adult- and childhood-onset systemic lupus erythematosus: a comparison of onset, clinical features, serology, and outcome. Br J Rheumatol 34:866–872PubMedCrossRef Tucker LB, Menon S, Schaller JG, Isenberg DA (1995) Adult- and childhood-onset systemic lupus erythematosus: a comparison of onset, clinical features, serology, and outcome. Br J Rheumatol 34:866–872PubMedCrossRef
3.
go back to reference Gardner-Medwin JM, Dolezalova P, Cummins C, Southwood TR (2002) Incidence of Henoch-Schonlein purpura, Kawasaki disease, and rare vasculitides in children of different ethnic origins. Lancet 360:1197–1202PubMedCrossRef Gardner-Medwin JM, Dolezalova P, Cummins C, Southwood TR (2002) Incidence of Henoch-Schonlein purpura, Kawasaki disease, and rare vasculitides in children of different ethnic origins. Lancet 360:1197–1202PubMedCrossRef
4.
go back to reference Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, Schaller JG, Talal N, Winchester RJ (1982) The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 25:1271–1277PubMedCrossRef Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, Schaller JG, Talal N, Winchester RJ (1982) The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 25:1271–1277PubMedCrossRef
5.
go back to reference Hersh AO, Trupin L, Yazdany J, Panopalis P, Julian L, Katz P, Criswell LA, Yelin E (2010) Childhood-onset disease as a predictor of mortality in an adult cohort of patients with systemic lupus erythematosus. Arthritis Care Res (Hoboken) 62:1152–1159CrossRef Hersh AO, Trupin L, Yazdany J, Panopalis P, Julian L, Katz P, Criswell LA, Yelin E (2010) Childhood-onset disease as a predictor of mortality in an adult cohort of patients with systemic lupus erythematosus. Arthritis Care Res (Hoboken) 62:1152–1159CrossRef
6.
go back to reference Hagelberg S, Lee Y, Bargman J, Mah G, Schneider R, Laskin C, Eddy A, Gladman D, Urowitz M, Hebert D, Silverman E (2002) Longterm followup of childhood lupus nephritis. J Rheumatol 29:2635–2642PubMed Hagelberg S, Lee Y, Bargman J, Mah G, Schneider R, Laskin C, Eddy A, Gladman D, Urowitz M, Hebert D, Silverman E (2002) Longterm followup of childhood lupus nephritis. J Rheumatol 29:2635–2642PubMed
7.
go back to reference Levy M, Montes de Oca M, Claude-Babron M (1994) Unfavorable outcomes (end-stage renal failure/death) in childhood onset systemic lupus erythematosus A multicenter study in Paris and its environs. Clin Exp Rheumatol 12(Suppl 10):S63–S68PubMedCrossRef Levy M, Montes de Oca M, Claude-Babron M (1994) Unfavorable outcomes (end-stage renal failure/death) in childhood onset systemic lupus erythematosus A multicenter study in Paris and its environs. Clin Exp Rheumatol 12(Suppl 10):S63–S68PubMedCrossRef
8.
go back to reference Watson L, Leone V, Pilkington C, Tullus K, Rangaraj S, McDonagh JE, Gardner-Medwin J, Wilkinson N, Riley P, Tizard J, Armon K, Sinha MD, Ioannou Y, Archer N, Bailey K, Davidson J, Baildam EM, Cleary G, McCann LJ, Beresford MW (2012) Juvenile-onset SLE; disease activity, severity and damage—the UK JSLE Cohort Study. Arthritis Rheum. doi:10.1002/art.34410 Watson L, Leone V, Pilkington C, Tullus K, Rangaraj S, McDonagh JE, Gardner-Medwin J, Wilkinson N, Riley P, Tizard J, Armon K, Sinha MD, Ioannou Y, Archer N, Bailey K, Davidson J, Baildam EM, Cleary G, McCann LJ, Beresford MW (2012) Juvenile-onset SLE; disease activity, severity and damage—the UK JSLE Cohort Study. Arthritis Rheum. doi:10.​1002/​art.​34410
9.
go back to reference Marini R, Costallat LT (1999) Young age at onset, renal involvement, and arterial hypertension are of adverse prognostic significance in juvenile systemic lupus erythematosus. Rev Rhum Engl Ed 66:303–309PubMed Marini R, Costallat LT (1999) Young age at onset, renal involvement, and arterial hypertension are of adverse prognostic significance in juvenile systemic lupus erythematosus. Rev Rhum Engl Ed 66:303–309PubMed
10.
go back to reference 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. J Am Soc Nephrol 15:241–250PubMedCrossRef 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. J Am Soc Nephrol 15:241–250PubMedCrossRef
11.
go back to reference Hiramatsu N, Kuroiwa T, Ikeuchi H, Maeshima A, Kaneko Y, Hiromura K, Ueki K, Nojima Y (2008) Revised classification of lupus nephritis is valuable in predicting renal outcome with an indication of the proportion of glomeruli affected by chronic lesions. Rheumatology (Oxford) 47:702–707CrossRef Hiramatsu N, Kuroiwa T, Ikeuchi H, Maeshima A, Kaneko Y, Hiromura K, Ueki K, Nojima Y (2008) Revised classification of lupus nephritis is valuable in predicting renal outcome with an indication of the proportion of glomeruli affected by chronic lesions. Rheumatology (Oxford) 47:702–707CrossRef
12.
go back to reference Marks SD, Tullus K, Sebire NJ (2006) Current issues in pediatric lupus nephritis: role of revised histopathological classification. Fetal Pediatr Pathol 25:297–309PubMedCrossRef Marks SD, Tullus K, Sebire NJ (2006) Current issues in pediatric lupus nephritis: role of revised histopathological classification. Fetal Pediatr Pathol 25:297–309PubMedCrossRef
13.
go back to reference Esdaile JM (1998) Current role of renal biopsy in patients with SLE. Baillieres Clin Rheumatol 12:433–448PubMedCrossRef Esdaile JM (1998) Current role of renal biopsy in patients with SLE. Baillieres Clin Rheumatol 12:433–448PubMedCrossRef
14.
go back to reference Askenazi D, Myones B, Kamdar A, Warren R, Perez M, De Guzman M, Minta A, Hicks MJ, Kale A (2007) Outcomes of children with proliferative lupus nephritis: the role of protocol renal biopsy. Pediatr Nephrol 22:981–986PubMedCrossRef Askenazi D, Myones B, Kamdar A, Warren R, Perez M, De Guzman M, Minta A, Hicks MJ, Kale A (2007) Outcomes of children with proliferative lupus nephritis: the role of protocol renal biopsy. Pediatr Nephrol 22:981–986PubMedCrossRef
15.
go back to reference Hiraki LT, Lu B, Alexander SR, Shaykevich T, Alarcon GS, Solomon DH, Winkelmayer WC, Costenbader KH (2011) End-stage renal disease due to lupus nephritis among children in the US, 1995–2006. Arthritis Rheum 63:1988–1997PubMedCrossRef Hiraki LT, Lu B, Alexander SR, Shaykevich T, Alarcon GS, Solomon DH, Winkelmayer WC, Costenbader KH (2011) End-stage renal disease due to lupus nephritis among children in the US, 1995–2006. Arthritis Rheum 63:1988–1997PubMedCrossRef
16.
go back to reference Ravelli A, Duarte-Salazar C, Buratti S, Reiff A, Bernstein B, Maldonado-Velazquez MR, Beristain-Manterola R, Maeno N, Takei S, Gerloni V, Spencer CH, Pratsidou-Gertsi P, Ruperto N, Pistorio A, Martini A (2003) Assessment of damage in juvenile-onset systemic lupus erythematosus: a multicenter cohort study. Arthritis Rheum 49:501–507PubMedCrossRef Ravelli A, Duarte-Salazar C, Buratti S, Reiff A, Bernstein B, Maldonado-Velazquez MR, Beristain-Manterola R, Maeno N, Takei S, Gerloni V, Spencer CH, Pratsidou-Gertsi P, Ruperto N, Pistorio A, Martini A (2003) Assessment of damage in juvenile-onset systemic lupus erythematosus: a multicenter cohort study. Arthritis Rheum 49:501–507PubMedCrossRef
17.
go back to reference Brunner HI, Gladman DD, Ibanez D, Urowitz MD, Silverman ED (2008) Difference in disease features between childhood-onset and adult-onset systemic lupus erythematosus. Arthritis Rheum 58:556–562PubMedCrossRef Brunner HI, Gladman DD, Ibanez D, Urowitz MD, Silverman ED (2008) Difference in disease features between childhood-onset and adult-onset systemic lupus erythematosus. Arthritis Rheum 58:556–562PubMedCrossRef
18.
go back to reference Mina R, von Scheven E, Ardoin SP, Eberhard BA, Punaro M, Ilowite N, Hsu J, Klein-Gitelman M, Moorthy LN, Muscal E, Radhakrishna SM, Wagner-Weiner L, Adams M, Blier P, Buckley L, Chalom E, Chedeville G, Eichenfield A, Fish N, Henrickson M, Hersh AO, Hollister R, Jones O, Jung L, Levy D, Lopez-Benitez J, McCurdy D, Miettunen PM, Quintero-Del Rio AI, Rothman D, Rullo O, Ruth N, Schanberg LE, Silverman E, Singer NG, Soep J, Syed R, Vogler LB, Yalcindag A, Yildirim-Toruner C, Wallace CA, Brunner HI (2012) Consensus treatment plans for induction therapy of newly diagnosed proliferative lupus nephritis in juvenile systemic lupus erythematosus. Arthritis Care Res (Hoboken) 64:375–383CrossRef Mina R, von Scheven E, Ardoin SP, Eberhard BA, Punaro M, Ilowite N, Hsu J, Klein-Gitelman M, Moorthy LN, Muscal E, Radhakrishna SM, Wagner-Weiner L, Adams M, Blier P, Buckley L, Chalom E, Chedeville G, Eichenfield A, Fish N, Henrickson M, Hersh AO, Hollister R, Jones O, Jung L, Levy D, Lopez-Benitez J, McCurdy D, Miettunen PM, Quintero-Del Rio AI, Rothman D, Rullo O, Ruth N, Schanberg LE, Silverman E, Singer NG, Soep J, Syed R, Vogler LB, Yalcindag A, Yildirim-Toruner C, Wallace CA, Brunner HI (2012) Consensus treatment plans for induction therapy of newly diagnosed proliferative lupus nephritis in juvenile systemic lupus erythematosus. Arthritis Care Res (Hoboken) 64:375–383CrossRef
19.
go back to reference Kazyra I, Pilkington C, Marks SD, Tullus K (2010) Mycophenolate mofetil treatment in children and adolescents with lupus. Arch Dis Child 95:1059–1061PubMedCrossRef Kazyra I, Pilkington C, Marks SD, Tullus K (2010) Mycophenolate mofetil treatment in children and adolescents with lupus. Arch Dis Child 95:1059–1061PubMedCrossRef
20.
go back to reference Pons-Estel GJ, Alarcon GS, McGwin G Jr, Danila MI, Zhang J, Bastian HM, Reveille JD, Vila LM (2009) Protective effect of hydroxychloroquine on renal damage in patients with lupus nephritis: LXV, data from a multiethnic US cohort. Arthritis Rheum 61:830–839PubMedCrossRef Pons-Estel GJ, Alarcon GS, McGwin G Jr, Danila MI, Zhang J, Bastian HM, Reveille JD, Vila LM (2009) Protective effect of hydroxychloroquine on renal damage in patients with lupus nephritis: LXV, data from a multiethnic US cohort. Arthritis Rheum 61:830–839PubMedCrossRef
21.
go back to reference Rovin BH, Furie R, Latinis K, Looney RJ, Fervenza FC, Sanchez-Guerrero J, Maciuca R, Zhang D, Garg JP, Brunetta P, Appel G (2012) Efficacy and safety of rituximab in patients with active proliferative lupus nephritis: The lupus nephritis assessment with rituximab (LUNAR) study. Arthritis Rheum 64:1215–1226. Rovin BH, Furie R, Latinis K, Looney RJ, Fervenza FC, Sanchez-Guerrero J, Maciuca R, Zhang D, Garg JP, Brunetta P, Appel G (2012) Efficacy and safety of rituximab in patients with active proliferative lupus nephritis: The lupus nephritis assessment with rituximab (LUNAR) study. Arthritis Rheum 64:1215–1226.
22.
go back to reference Pepper R, Griffith M, Kirwan C, Levy J, Taube D, Pusey C, Lightstone L, Cairns T (2009) Rituximab is an effective treatment for lupus nephritis and allows a reduction in maintenance steroids. Nephrol Dial Transplant 24:3717–3723PubMedCrossRef Pepper R, Griffith M, Kirwan C, Levy J, Taube D, Pusey C, Lightstone L, Cairns T (2009) Rituximab is an effective treatment for lupus nephritis and allows a reduction in maintenance steroids. Nephrol Dial Transplant 24:3717–3723PubMedCrossRef
23.
go back to reference Podolskaya A, Stadermann M, Pilkington C, Marks SD, Tullus K (2008) B cell depletion therapy for 19 patients with refractory systemic lupus erythematosus. Arch Dis Child 93:401–406PubMedCrossRef Podolskaya A, Stadermann M, Pilkington C, Marks SD, Tullus K (2008) B cell depletion therapy for 19 patients with refractory systemic lupus erythematosus. Arch Dis Child 93:401–406PubMedCrossRef
24.
go back to reference Mak A, Mok CC, Chu WP, To CH, Wong SN, Au TC (2007) Renal damage in systemic lupus erythematosus: a comparative analysis of different age groups. Lupus 16:28–34PubMedCrossRef Mak A, Mok CC, Chu WP, To CH, Wong SN, Au TC (2007) Renal damage in systemic lupus erythematosus: a comparative analysis of different age groups. Lupus 16:28–34PubMedCrossRef
25.
go back to reference Norby GE, Strom EH, Midtvedt K, Hartmann A, Gilboe IM, Leivestad T, Stenstrom J, Holdaas H (2010) Recurrent lupus nephritis after kidney transplantation: a surveillance biopsy study. Ann Rheum Dis 69:1484–1487PubMedCrossRef Norby GE, Strom EH, Midtvedt K, Hartmann A, Gilboe IM, Leivestad T, Stenstrom J, Holdaas H (2010) Recurrent lupus nephritis after kidney transplantation: a surveillance biopsy study. Ann Rheum Dis 69:1484–1487PubMedCrossRef
26.
go back to reference Isenberg DA, Rahman A, Allen E, Farewell V, Akil M, Bruce IN, D'Cruz D, Griffiths B, Khamashta M, Maddison P, McHugh N, Snaith M, The LS, Yee CS, Zoma A, Gordon C (2005) BILAG 2004. Development and initial validation of an updated version of the British Isles Lupus Assessment Group's disease activity index for patients with systemic lupus erythematosus. Rheumatology (Oxford) 44:902–906CrossRef Isenberg DA, Rahman A, Allen E, Farewell V, Akil M, Bruce IN, D'Cruz D, Griffiths B, Khamashta M, Maddison P, McHugh N, Snaith M, The LS, Yee CS, Zoma A, Gordon C (2005) BILAG 2004. Development and initial validation of an updated version of the British Isles Lupus Assessment Group's disease activity index for patients with systemic lupus erythematosus. Rheumatology (Oxford) 44:902–906CrossRef
27.
go back to reference Gladman DD, Ibanez D, Urowitz MB (2002) Systemic lupus erythematosus disease activity index 2000. J Rheumatol 29:288–291PubMed Gladman DD, Ibanez D, Urowitz MB (2002) Systemic lupus erythematosus disease activity index 2000. J Rheumatol 29:288–291PubMed
28.
go back to reference Siedner MJ, Gelber AC, Rovin BH, McKinley AM, Christopher-Stine L, Astor B, Petri M, Fine DM (2008) Diagnostic accuracy study of urine dipstick in relation to 24-hour measurement as a screening tool for proteinuria in lupus nephritis. J Rheumatol 35:84–90PubMed Siedner MJ, Gelber AC, Rovin BH, McKinley AM, Christopher-Stine L, Astor B, Petri M, Fine DM (2008) Diagnostic accuracy study of urine dipstick in relation to 24-hour measurement as a screening tool for proteinuria in lupus nephritis. J Rheumatol 35:84–90PubMed
29.
go back to reference Cottiero RA, Madaio MP, Levey AS (1995) Glomerular filtration rate and urinary albumin excretion rate in systemic lupus erythematosus. Nephron 69:140–146PubMedCrossRef Cottiero RA, Madaio MP, Levey AS (1995) Glomerular filtration rate and urinary albumin excretion rate in systemic lupus erythematosus. Nephron 69:140–146PubMedCrossRef
30.
go back to reference Leung YY, Szeto CC, Tam LS, Lam CW, Li EK, Wong KC, Yu SW, Kun EW (2007) Urine protein-to-creatinine ratio in an untimed urine collection is a reliable measure of proteinuria in lupus nephritis. Rheumatology (Oxford) 46:649–652CrossRef Leung YY, Szeto CC, Tam LS, Lam CW, Li EK, Wong KC, Yu SW, Kun EW (2007) Urine protein-to-creatinine ratio in an untimed urine collection is a reliable measure of proteinuria in lupus nephritis. Rheumatology (Oxford) 46:649–652CrossRef
31.
go back to reference Christopher-Stine L, Siedner M, Lin J, Haas M, Parekh H, Petri M, Fine DM (2007) Renal biopsy in lupus patients with low levels of proteinuria. J Rheumatol 34:332–335PubMed Christopher-Stine L, Siedner M, Lin J, Haas M, Parekh H, Petri M, Fine DM (2007) Renal biopsy in lupus patients with low levels of proteinuria. J Rheumatol 34:332–335PubMed
32.
go back to reference Fine DM, Ziegenbein M, Petri M, Han EC, McKinley AM, Chellini JW, Nagaraja HN, Carson KA, Rovin BH (2009) A prospective study of protein excretion using short-interval timed urine collections in patients with lupus nephritis. Kidney Int 76:1284–1288PubMedCrossRef Fine DM, Ziegenbein M, Petri M, Han EC, McKinley AM, Chellini JW, Nagaraja HN, Carson KA, Rovin BH (2009) A prospective study of protein excretion using short-interval timed urine collections in patients with lupus nephritis. Kidney Int 76:1284–1288PubMedCrossRef
33.
go back to reference Schwartz GJ, Haycock GB, Edelmann CM Jr, Spitzer A (1976) A simple estimate of glomerular filtration rate in children derived from body length and plasma creatinine. Pediatrics 58:259–263PubMed Schwartz GJ, Haycock GB, Edelmann CM Jr, Spitzer A (1976) A simple estimate of glomerular filtration rate in children derived from body length and plasma creatinine. Pediatrics 58:259–263PubMed
34.
go back to reference Ayodele OE, Okpechi IG, Swanepoel CR (2010) Predictors of poor renal outcome in patients with biopsy-proven lupus nephritis. Nephrology (Carlton) 15:482–490CrossRef Ayodele OE, Okpechi IG, Swanepoel CR (2010) Predictors of poor renal outcome in patients with biopsy-proven lupus nephritis. Nephrology (Carlton) 15:482–490CrossRef
35.
go back to reference Woolf A, Croker B, Osofsky SG, Kredich DW (1979) Nephritis in children and young adults with systemic lupus erythematosus and normal urinary sediment. Pediatrics 64:678–685PubMed Woolf A, Croker B, Osofsky SG, Kredich DW (1979) Nephritis in children and young adults with systemic lupus erythematosus and normal urinary sediment. Pediatrics 64:678–685PubMed
36.
go back to reference Nasiri S, Karimifar M, Bonakdar ZS, Salesi M (2010) Correlation of ESR, C3, C4, anti-DNA and lupus activity based on British Isles Lupus Assessment Group Index in patients of rheumatology clinic. Rheumatol Int 30:1605–1609PubMedCrossRef Nasiri S, Karimifar M, Bonakdar ZS, Salesi M (2010) Correlation of ESR, C3, C4, anti-DNA and lupus activity based on British Isles Lupus Assessment Group Index in patients of rheumatology clinic. Rheumatol Int 30:1605–1609PubMedCrossRef
37.
go back to reference Kasitanon N, Magder LS, Petri M (2006) Predictors of survival in systemic lupus erythematosus. Medicine (Baltimore) 85:147–156CrossRef Kasitanon N, Magder LS, Petri M (2006) Predictors of survival in systemic lupus erythematosus. Medicine (Baltimore) 85:147–156CrossRef
38.
go back to reference Moroni G, Radice A, Giammarresi G, Quaglini S, Gallelli B, Leoni A, Li Vecchi M, 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 68:234–237PubMedCrossRef Moroni G, Radice A, Giammarresi G, Quaglini S, Gallelli B, Leoni A, Li Vecchi M, 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 68:234–237PubMedCrossRef
39.
go back to reference Welch TR, Blystone LW (2009) Renal disease associated with inherited disorders of the complement system. Pediatr Nephrol 24:1439–1444PubMedCrossRef Welch TR, Blystone LW (2009) Renal disease associated with inherited disorders of the complement system. Pediatr Nephrol 24:1439–1444PubMedCrossRef
40.
go back to reference Al-Mayouf SM, Abanomi H, Eldali A (2011) Impact of C1q deficiency on the severity and outcome of childhood systemic lupus erythematosus. Int J Rheum Dis 14:81–85PubMedCrossRef Al-Mayouf SM, Abanomi H, Eldali A (2011) Impact of C1q deficiency on the severity and outcome of childhood systemic lupus erythematosus. Int J Rheum Dis 14:81–85PubMedCrossRef
41.
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 1173:235–238PubMedCrossRef 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 1173:235–238PubMedCrossRef
42.
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 20:1267–1274PubMedCrossRef 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 20:1267–1274PubMedCrossRef
43.
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 20:28–34PubMedCrossRef 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 20:28–34PubMedCrossRef
44.
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 63:2436–2444PubMedCrossRef 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 63:2436–2444PubMedCrossRef
45.
go back to reference Eriksson C, Kokkonen H, Johansson M, Hallmans G, Wadell G, Rantapaa-Dahlqvist S (2011) Autoantibodies predate the onset of systemic lupus erythematosus in northern Sweden. Arthritis Res Ther 13:30CrossRef Eriksson C, Kokkonen H, Johansson M, Hallmans G, Wadell G, Rantapaa-Dahlqvist S (2011) Autoantibodies predate the onset of systemic lupus erythematosus in northern Sweden. Arthritis Res Ther 13:30CrossRef
46.
go back to reference Campos LM, Kiss MH, Scheinberg MA, Mangueira CL, Silva CA (2006) Antinucleosome antibodies in patients with juvenile systemic lupus erythematosus. Lupus 15:496–500PubMedCrossRef Campos LM, Kiss MH, Scheinberg MA, Mangueira CL, Silva CA (2006) Antinucleosome antibodies in patients with juvenile systemic lupus erythematosus. Lupus 15:496–500PubMedCrossRef
47.
go back to reference Biomarkers Definitions Working Group (2001) Biomarkers and surrogate endpoints: preferred definitions and conceptual framework. Clin Pharmacol Ther 69:89–95CrossRef Biomarkers Definitions Working Group (2001) Biomarkers and surrogate endpoints: preferred definitions and conceptual framework. Clin Pharmacol Ther 69:89–95CrossRef
48.
go back to reference Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH (1992) Derivation of the SLEDAI. A disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. Arthritis Rheum 35:630–640PubMedCrossRef Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH (1992) Derivation of the SLEDAI. A disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. Arthritis Rheum 35:630–640PubMedCrossRef
49.
go back to reference Marks SD, Shah V, Pilkington C, Tullus K (2010) Urinary monocyte chemoattractant protein-1 correlates with disease activity in lupus nephritis. Pediatr Nephrol 25:2283–2288PubMedCrossRef Marks SD, Shah V, Pilkington C, Tullus K (2010) Urinary monocyte chemoattractant protein-1 correlates with disease activity in lupus nephritis. Pediatr Nephrol 25:2283–2288PubMedCrossRef
50.
go back to reference Rovin BH, Song H, Birmingham DJ, Hebert LA, Yu CY, Nagaraja HN (2005) Urine chemokines as biomarkers of human systemic lupus erythematosus activity. J Am Soc Nephrol 16:467–473PubMedCrossRef Rovin BH, Song H, Birmingham DJ, Hebert LA, Yu CY, Nagaraja HN (2005) Urine chemokines as biomarkers of human systemic lupus erythematosus activity. J Am Soc Nephrol 16:467–473PubMedCrossRef
51.
go back to reference Gwira JA, Wei F, Ishibe S, Ueland JM, Barasch J, Cantley LG (2005) Expression of neutrophil gelatinase-associated lipocalin regulates epithelial morphogenesis in vitro. J Biol Chem 280:7875–7882PubMedCrossRef Gwira JA, Wei F, Ishibe S, Ueland JM, Barasch J, Cantley LG (2005) Expression of neutrophil gelatinase-associated lipocalin regulates epithelial morphogenesis in vitro. J Biol Chem 280:7875–7882PubMedCrossRef
52.
go back to reference Trachtman H, Christen E, Cnaan A, Patrick J, Mai V, Mishra J, Jain A, Bullington N, Devarajan P (2006) Urinary neutrophil gelatinase-associated lipocalcin in D + HUS: a novel marker of renal injury. Pediatr Nephrol 21:989–994PubMedCrossRef Trachtman H, Christen E, Cnaan A, Patrick J, Mai V, Mishra J, Jain A, Bullington N, Devarajan P (2006) Urinary neutrophil gelatinase-associated lipocalcin in D + HUS: a novel marker of renal injury. Pediatr Nephrol 21:989–994PubMedCrossRef
53.
go back to reference Hollmen ME, Kyllonen LE, Inkinen KA, Lalla ML, Salmela KT (2011) Urine neutrophil gelatinase-associated lipocalin is a marker of graft recovery after kidney transplantation. Kidney Int 79:89–98PubMedCrossRef Hollmen ME, Kyllonen LE, Inkinen KA, Lalla ML, Salmela KT (2011) Urine neutrophil gelatinase-associated lipocalin is a marker of graft recovery after kidney transplantation. Kidney Int 79:89–98PubMedCrossRef
54.
go back to reference Haase M, Bellomo R, Devarajan P, Schlattmann P, Haase-Fielitz A (2009) Accuracy of neutrophil gelatinase-associated lipocalin (NGAL) in diagnosis and prognosis in acute kidney injury: a systematic review and meta-analysis. Am J Kidney Dis 54:1012–1024PubMedCrossRef Haase M, Bellomo R, Devarajan P, Schlattmann P, Haase-Fielitz A (2009) Accuracy of neutrophil gelatinase-associated lipocalin (NGAL) in diagnosis and prognosis in acute kidney injury: a systematic review and meta-analysis. Am J Kidney Dis 54:1012–1024PubMedCrossRef
55.
go back to reference Viau A, El Karoui K, Laouari D, Burtin M, Nguyen C, Mori K, Pillebout E, Berger T, Mak TW, Knebelmann B, Friedlander G, Barasch J, Terzi F (2010) Lipocalin 2 is essential for chronic kidney disease progression in mice and humans. J Clin Invest 120:4065–4076PubMedCrossRef Viau A, El Karoui K, Laouari D, Burtin M, Nguyen C, Mori K, Pillebout E, Berger T, Mak TW, Knebelmann B, Friedlander G, Barasch J, Terzi F (2010) Lipocalin 2 is essential for chronic kidney disease progression in mice and humans. J Clin Invest 120:4065–4076PubMedCrossRef
56.
go back to reference Pawar RD, Pitashny M, Gindea S, Tan Tieng A, Levine B, Goilav B, Campbell SR, Xia Y, Qing X, Thomas D, Herlitz L, Berger T, Mak TM, Putterman C (2012) Neutrophil gelatinase associated lipocalin is instrumental in the pathogenesis of antibody-mediated nephritis. Arthritis Rheum. 64:1620–1631. Pawar RD, Pitashny M, Gindea S, Tan Tieng A, Levine B, Goilav B, Campbell SR, Xia Y, Qing X, Thomas D, Herlitz L, Berger T, Mak TM, Putterman C (2012) Neutrophil gelatinase associated lipocalin is instrumental in the pathogenesis of antibody-mediated nephritis. Arthritis Rheum. 64:1620–1631.
57.
go back to reference Brunner HI, Mueller M, Rutherford C, Passo MH, Witte D, Grom A, Mishra J, Devarajan P (2006) Urinary neutrophil gelatinase-associated lipocalin as a biomarker of nephritis in childhood-onset systemic lupus erythematosus. Arthritis Rheum 54:2577–2584PubMedCrossRef Brunner HI, Mueller M, Rutherford C, Passo MH, Witte D, Grom A, Mishra J, Devarajan P (2006) Urinary neutrophil gelatinase-associated lipocalin as a biomarker of nephritis in childhood-onset systemic lupus erythematosus. Arthritis Rheum 54:2577–2584PubMedCrossRef
58.
go back to reference Rubinstein T, Pitashny M, Levine B, Schwartz N, Schwartzman J, Weinstein E, Pego-Reigosa JM, Lu TY, Isenberg D, Rahman A, Putterman C (2010) Urinary neutrophil gelatinase-associated lipocalin as a novel biomarker for disease activity in lupus nephritis. Rheumatology (Oxford) 49:960–971CrossRef Rubinstein T, Pitashny M, Levine B, Schwartz N, Schwartzman J, Weinstein E, Pego-Reigosa JM, Lu TY, Isenberg D, Rahman A, Putterman C (2010) Urinary neutrophil gelatinase-associated lipocalin as a novel biomarker for disease activity in lupus nephritis. Rheumatology (Oxford) 49:960–971CrossRef
59.
go back to reference Suzuki M, Wiers KM, Klein-Gitelman MS, Haines KA, Olson J, Onel KB, O'Neil K, Passo MH, Singer NG, Tucker L, Ying J, Devarajan P, Brunner HI (2008) Neutrophil gelatinase-associated lipocalin as a biomarker of disease activity in pediatric lupus nephritis. Pediatr Nephrol 23:403–412PubMedCrossRef Suzuki M, Wiers KM, Klein-Gitelman MS, Haines KA, Olson J, Onel KB, O'Neil K, Passo MH, Singer NG, Tucker L, Ying J, Devarajan P, Brunner HI (2008) Neutrophil gelatinase-associated lipocalin as a biomarker of disease activity in pediatric lupus nephritis. Pediatr Nephrol 23:403–412PubMedCrossRef
60.
go back to reference Hinze CH, Suzuki M, Klein-Gitelman M, Passo MH, Olson J, Singer NG, Haines KA, Onel K, O'Neil K, Silverman ED, Tucker L, Ying J, Devarajan P, Brunner HI (2009) Neutrophil gelatinase-associated lipocalin is a predictor of the course of global and renal childhood-onset systemic lupus erythematosus disease activity. Arthritis Rheum 60:2772–2781PubMedCrossRef Hinze CH, Suzuki M, Klein-Gitelman M, Passo MH, Olson J, Singer NG, Haines KA, Onel K, O'Neil K, Silverman ED, Tucker L, Ying J, Devarajan P, Brunner HI (2009) Neutrophil gelatinase-associated lipocalin is a predictor of the course of global and renal childhood-onset systemic lupus erythematosus disease activity. Arthritis Rheum 60:2772–2781PubMedCrossRef
61.
go back to reference Yilmaz A, Sevketoglu E, Gedikbasi A, Karyagar S, Kiyak A, Mulazimoglu M, Aydogan G, Ozpacaci T, Hatipoglu S (2009) Early prediction of urinary tract infection with urinary neutrophil gelatinase associated lipocalin. Pediatr Nephrol 24:2387–2392PubMedCrossRef Yilmaz A, Sevketoglu E, Gedikbasi A, Karyagar S, Kiyak A, Mulazimoglu M, Aydogan G, Ozpacaci T, Hatipoglu S (2009) Early prediction of urinary tract infection with urinary neutrophil gelatinase associated lipocalin. Pediatr Nephrol 24:2387–2392PubMedCrossRef
62.
go back to reference Matoba K, Kawanami D, Ishizawa S, Kanazawa Y, Yokota T, Utsunomiya K (2010) Rho-kinase mediates TNF-alpha-induced MCP-1 expression via p38 MAPK signaling pathway in mesangial cells. Biochem Biophys Res Commun 402:725–730PubMedCrossRef Matoba K, Kawanami D, Ishizawa S, Kanazawa Y, Yokota T, Utsunomiya K (2010) Rho-kinase mediates TNF-alpha-induced MCP-1 expression via p38 MAPK signaling pathway in mesangial cells. Biochem Biophys Res Commun 402:725–730PubMedCrossRef
63.
go back to reference Tarabra E, Giunti S, Barutta F, Salvidio G, Burt D, Deferrari G, Gambino R, Vergola D, Pinach S, Perin PC, Camussi G, Gruden G (2009) Effect of the monocyte chemoattractant protein-1/CC chemokine receptor 2 system on nephrin expression in streptozotocin-treated mice and human cultured podocytes. Diabetes 58:2109–2118PubMedCrossRef Tarabra E, Giunti S, Barutta F, Salvidio G, Burt D, Deferrari G, Gambino R, Vergola D, Pinach S, Perin PC, Camussi G, Gruden G (2009) Effect of the monocyte chemoattractant protein-1/CC chemokine receptor 2 system on nephrin expression in streptozotocin-treated mice and human cultured podocytes. Diabetes 58:2109–2118PubMedCrossRef
64.
go back to reference Marks SD, Williams SJ, Tullus K, Sebire NJ (2008) Glomerular expression of monocyte chemoattractant protein-1 is predictive of poor renal prognosis in pediatric lupus nephritis. Nephrol Dial Transpl 23:3521–3526CrossRef Marks SD, Williams SJ, Tullus K, Sebire NJ (2008) Glomerular expression of monocyte chemoattractant protein-1 is predictive of poor renal prognosis in pediatric lupus nephritis. Nephrol Dial Transpl 23:3521–3526CrossRef
65.
go back to reference Wada T, Yokoyama H, Su SB, Mukaida N, Iwano M, Dohi K, Takahashi Y, Sasaki T, Furuichi K, Segawa C, Hisada Y, Ohta S, Takasawa K, Kobayashi K, Matsushima K (1996) Monitoring urinary levels of monocyte chemotactic and activating factor reflects disease activity of lupus nephritis. Kidney Int 49:761–767PubMedCrossRef Wada T, Yokoyama H, Su SB, Mukaida N, Iwano M, Dohi K, Takahashi Y, Sasaki T, Furuichi K, Segawa C, Hisada Y, Ohta S, Takasawa K, Kobayashi K, Matsushima K (1996) Monitoring urinary levels of monocyte chemotactic and activating factor reflects disease activity of lupus nephritis. Kidney Int 49:761–767PubMedCrossRef
66.
go back to reference El-Shehaby A, Darweesh H, El-Khatib M, Momtaz M, Marzouk S, El-Shaarawy N, Emad Y (2011) Correlations of urinary biomarkers, TNF-like weak inducer of apoptosis (TWEAK), osteoprotegerin (OPG), monocyte chemoattractant protein-1 (MCP-1), and IL-8 with lupus nephritis. J Clin Immunol 31:848–856PubMedCrossRef El-Shehaby A, Darweesh H, El-Khatib M, Momtaz M, Marzouk S, El-Shaarawy N, Emad Y (2011) Correlations of urinary biomarkers, TNF-like weak inducer of apoptosis (TWEAK), osteoprotegerin (OPG), monocyte chemoattractant protein-1 (MCP-1), and IL-8 with lupus nephritis. J Clin Immunol 31:848–856PubMedCrossRef
67.
go back to reference Watson L, Midgley A, Pilkington C, Tullus K, Marks SD, Holt RC, Jones CA, Beresford MW (2011) Urinary monocyte chemoattractant protein 1 and alpha 1 acid glycoprotein as biomarkers of renal disease activity in juvenile-onset systemic lupus erythematosus. Lupus 21:496–501PubMedCrossRef Watson L, Midgley A, Pilkington C, Tullus K, Marks SD, Holt RC, Jones CA, Beresford MW (2011) Urinary monocyte chemoattractant protein 1 and alpha 1 acid glycoprotein as biomarkers of renal disease activity in juvenile-onset systemic lupus erythematosus. Lupus 21:496–501PubMedCrossRef
68.
go back to reference Szeto CC, Chan RW, Lai KB, Szeto CY, Chow KM, Li PK, Lai FM (2005) Messenger RNA expression of target genes in the urinary sediment of patients with chronic kidney diseases. Nephrol Dial Transplant 20:105–113PubMedCrossRef Szeto CC, Chan RW, Lai KB, Szeto CY, Chow KM, Li PK, Lai FM (2005) Messenger RNA expression of target genes in the urinary sediment of patients with chronic kidney diseases. Nephrol Dial Transplant 20:105–113PubMedCrossRef
69.
go back to reference Avihingsanon Y, Phumesin P, Benjachat T, Akkasilpa S, Kittikowit V, Praditpornsilpa K, Wongpiyabavorn J, Eiam-Ong S, Hemachudha T, Tungsanga K, Hirankarn N (2006) Measurement of urinary chemokine and growth factor messenger RNAs: a noninvasive monitoring in lupus nephritis. Kidney Int 69:747–753PubMedCrossRef Avihingsanon Y, Phumesin P, Benjachat T, Akkasilpa S, Kittikowit V, Praditpornsilpa K, Wongpiyabavorn J, Eiam-Ong S, Hemachudha T, Tungsanga K, Hirankarn N (2006) Measurement of urinary chemokine and growth factor messenger RNAs: a noninvasive monitoring in lupus nephritis. Kidney Int 69:747–753PubMedCrossRef
70.
go back to reference Hammad AM, Youssef HM, El-Arman MM (2006) Transforming growth factor beta 1 in children with systemic lupus erythematosus: a possible relation with clinical presentation of lupus nephritis. Lupus 15:608–612PubMedCrossRef Hammad AM, Youssef HM, El-Arman MM (2006) Transforming growth factor beta 1 in children with systemic lupus erythematosus: a possible relation with clinical presentation of lupus nephritis. Lupus 15:608–612PubMedCrossRef
71.
go back to reference Marks SD, Shah V, Pilkington C, Woo P, Dillon MJ (2005) Renal tubular dysfunction in children with systemic lupus erythematosus. Pediatr Nephrol 20:141–148PubMedCrossRef Marks SD, Shah V, Pilkington C, Woo P, Dillon MJ (2005) Renal tubular dysfunction in children with systemic lupus erythematosus. Pediatr Nephrol 20:141–148PubMedCrossRef
72.
go back to reference Erdener D, Aksu K, Bicer I, Doganavsargil E, Kutay FZ (2005) Urinary N-acetyl-beta-D-glucosaminidase (NAG) in lupus nephritis and rheumatoid arthritis. J Clin Lab Anal 19:172–176PubMedCrossRef Erdener D, Aksu K, Bicer I, Doganavsargil E, Kutay FZ (2005) Urinary N-acetyl-beta-D-glucosaminidase (NAG) in lupus nephritis and rheumatoid arthritis. J Clin Lab Anal 19:172–176PubMedCrossRef
73.
go back to reference Sesso R, Rettori R, Nishida S, Sato E, Ajzen H, Pereira AB (1994) Assessment of lupus nephritis activity using urinary retinol-binding protein. Nephrol Dial Transplant 9:367–371PubMed Sesso R, Rettori R, Nishida S, Sato E, Ajzen H, Pereira AB (1994) Assessment of lupus nephritis activity using urinary retinol-binding protein. Nephrol Dial Transplant 9:367–371PubMed
74.
go back to reference Skalova S, Rejtar P, Kutilek S (2009) Urinary N-acetyl-beta-D-glucosaminidase (U-NAG) activity in children with vesicoureteral reflux. Bratisl Lek Listy 110:69–72PubMed Skalova S, Rejtar P, Kutilek S (2009) Urinary N-acetyl-beta-D-glucosaminidase (U-NAG) activity in children with vesicoureteral reflux. Bratisl Lek Listy 110:69–72PubMed
75.
go back to reference Florkowski CM, Jones AF, Guy JM, Husband DJ, Stevens J (1994) Retinol binding proteinuria and phosphaturia: markers of paracetamol-induced nephrotoxicity. Ann Clin Biochem 31:331–334PubMed Florkowski CM, Jones AF, Guy JM, Husband DJ, Stevens J (1994) Retinol binding proteinuria and phosphaturia: markers of paracetamol-induced nephrotoxicity. Ann Clin Biochem 31:331–334PubMed
76.
go back to reference Suzuki M, Wiers K, Brooks EB, Greis KD, Haines K, Klein-Gitelman MS, Olson J, Onel K, O'Neil KM, Silverman ED, Tucker L, Ying J, Devarajan P, Brunner HI (2009) Initial validation of a novel protein biomarker panel for active pediatric lupus nephritis. Pediatr Res 65:530–536PubMedCrossRef Suzuki M, Wiers K, Brooks EB, Greis KD, Haines K, Klein-Gitelman MS, Olson J, Onel K, O'Neil KM, Silverman ED, Tucker L, Ying J, Devarajan P, Brunner HI (2009) Initial validation of a novel protein biomarker panel for active pediatric lupus nephritis. Pediatr Res 65:530–536PubMedCrossRef
77.
go back to reference Bauer JW, Petri M, Batliwalla FM, Koeuth T, Wilson J, Slattery C, Panoskaltsis-Mortari A, Gregersen PK, Behrens TW, Baechler EC (2009) Interferon-regulated chemokines as biomarkers of systemic lupus erythematosus disease activity: a validation study. Arthritis Rheum 60:3098–3107PubMedCrossRef Bauer JW, Petri M, Batliwalla FM, Koeuth T, Wilson J, Slattery C, Panoskaltsis-Mortari A, Gregersen PK, Behrens TW, Baechler EC (2009) Interferon-regulated chemokines as biomarkers of systemic lupus erythematosus disease activity: a validation study. Arthritis Rheum 60:3098–3107PubMedCrossRef
78.
go back to reference Lu J, Kwan BC, Lai FM, Choi PC, Tam LS, Li EK, Chow KM, Wang G, Li PK, Szeto CC (2011) Gene expression of TWEAK/Fn14 and IP-10/CXCR3 in glomerulus and tubulointerstitium of patients with lupus nephritis. Nephrology (Carlton) 16:426–432CrossRef Lu J, Kwan BC, Lai FM, Choi PC, Tam LS, Li EK, Chow KM, Wang G, Li PK, Szeto CC (2011) Gene expression of TWEAK/Fn14 and IP-10/CXCR3 in glomerulus and tubulointerstitium of patients with lupus nephritis. Nephrology (Carlton) 16:426–432CrossRef
79.
go back to reference Sanz AB, Sanchez-Nino MD, Ortiz A (2011) TWEAK, a multifunctional cytokine in kidney injury. Kidney Int 80:708–718PubMedCrossRef Sanz AB, Sanchez-Nino MD, Ortiz A (2011) TWEAK, a multifunctional cytokine in kidney injury. Kidney Int 80:708–718PubMedCrossRef
80.
go back to reference Schwartz N, Rubinstein T, Burkly LC, Collins CE, Blanco I, Su L, Hojaili B, Mackay M, Aranow C, Stohl W, Rovin BH, Michaelson JS, Putterman C (2009) Urinary TWEAK as a biomarker of lupus nephritis: a multicenter cohort study. Arthritis Res Ther 11:143CrossRef Schwartz N, Rubinstein T, Burkly LC, Collins CE, Blanco I, Su L, Hojaili B, Mackay M, Aranow C, Stohl W, Rovin BH, Michaelson JS, Putterman C (2009) Urinary TWEAK as a biomarker of lupus nephritis: a multicenter cohort study. Arthritis Res Ther 11:143CrossRef
81.
go back to reference Yokoyama H, Takaeda M, Wada T, Ohta S, Hisada Y, Segawa C, Furuichi K, Kobayashi K (1997) Glomerular ICAM-1 expression related to circulating TNF-alpha in human glomerulonephritis. Nephron 76:425–433PubMedCrossRef Yokoyama H, Takaeda M, Wada T, Ohta S, Hisada Y, Segawa C, Furuichi K, Kobayashi K (1997) Glomerular ICAM-1 expression related to circulating TNF-alpha in human glomerulonephritis. Nephron 76:425–433PubMedCrossRef
82.
go back to reference Abd-Elkareem MI, Al Tamimy HM, Khamis OA, Abdellatif SS, Hussein MR (2010) Increased urinary levels of the leukocyte adhesion molecules ICAM-1 and VCAM-1 in human lupus nephritis with advanced renal histological changes: preliminary findings. Clin Exp Nephrol 14:548–557PubMedCrossRef Abd-Elkareem MI, Al Tamimy HM, Khamis OA, Abdellatif SS, Hussein MR (2010) Increased urinary levels of the leukocyte adhesion molecules ICAM-1 and VCAM-1 in human lupus nephritis with advanced renal histological changes: preliminary findings. Clin Exp Nephrol 14:548–557PubMedCrossRef
83.
go back to reference Molad Y, Miroshnik E, Sulkes J, Pitlik S, Weinberger A, Monselise Y (2002) Urinary soluble VCAM-1 in systemic lupus erythematosus: a clinical marker for monitoring disease activity and damage. Clin Exp Rheumatol 20:403–406PubMed Molad Y, Miroshnik E, Sulkes J, Pitlik S, Weinberger A, Monselise Y (2002) Urinary soluble VCAM-1 in systemic lupus erythematosus: a clinical marker for monitoring disease activity and damage. Clin Exp Rheumatol 20:403–406PubMed
84.
go back to reference Zhang X, Jin M, Wu H, Nadasdy T, Nadasdy G, Harris N, Green-Church K, Nagaraja H, Birmingham DJ, Yu CY, Hebert LA, Rovin BH (2008) Biomarkers of lupus nephritis determined by serial urine proteomics. Kidney Int 74:799–807PubMedCrossRef Zhang X, Jin M, Wu H, Nadasdy T, Nadasdy G, Harris N, Green-Church K, Nagaraja H, Birmingham DJ, Yu CY, Hebert LA, Rovin BH (2008) Biomarkers of lupus nephritis determined by serial urine proteomics. Kidney Int 74:799–807PubMedCrossRef
85.
go back to reference Varghese SA, Powell TB, Budisavljevic MN, Oates JC, Raymond JR, Almeida JS, Arthur JM (2007) Urine biomarkers predict the cause of glomerular disease. J Am Soc Nephrol 18:913–922PubMedCrossRef Varghese SA, Powell TB, Budisavljevic MN, Oates JC, Raymond JR, Almeida JS, Arthur JM (2007) Urine biomarkers predict the cause of glomerular disease. J Am Soc Nephrol 18:913–922PubMedCrossRef
86.
go back to reference Suzuki M, Ross GF, Wiers K, Nelson S, Bennett M, Passo MH, Devarajan P, Brunner HI (2007) Identification of a urinary proteomic signature for lupus nephritis in children. Pediatr Nephrol 22:2047–2057PubMedCrossRef Suzuki M, Ross GF, Wiers K, Nelson S, Bennett M, Passo MH, Devarajan P, Brunner HI (2007) Identification of a urinary proteomic signature for lupus nephritis in children. Pediatr Nephrol 22:2047–2057PubMedCrossRef
87.
go back to reference Fu Q, Chen X, Cui H, Guo Y, Chen J, Shen N, Bao C (2008) Association of elevated transcript levels of interferon-inducible chemokines with disease activity and organ damage in systemic lupus erythematosus patients. Arthritis Res Ther 10:112CrossRef Fu Q, Chen X, Cui H, Guo Y, Chen J, Shen N, Bao C (2008) Association of elevated transcript levels of interferon-inducible chemokines with disease activity and organ damage in systemic lupus erythematosus patients. Arthritis Res Ther 10:112CrossRef
88.
go back to reference Chan RW, Tam LS, Li EK, Lai FM, Chow KM, Lai KB, Li PK, Szeto CC (2003) Inflammatory cytokine gene expression in the urinary sediment of patients with lupus nephritis. Arthritis Rheum 48:1326–1331PubMedCrossRef Chan RW, Tam LS, Li EK, Lai FM, Chow KM, Lai KB, Li PK, Szeto CC (2003) Inflammatory cytokine gene expression in the urinary sediment of patients with lupus nephritis. Arthritis Rheum 48:1326–1331PubMedCrossRef
89.
go back to reference Chan RW, Lai FM, Li EK, Tam LS, Chow KM, Lai KB, Li PK, Szeto CC (2007) Intrarenal cytokine gene expression in lupus nephritis. Ann Rheum Dis 66:886–892PubMedCrossRef Chan RW, Lai FM, Li EK, Tam LS, Chow KM, Lai KB, Li PK, Szeto CC (2007) Intrarenal cytokine gene expression in lupus nephritis. Ann Rheum Dis 66:886–892PubMedCrossRef
90.
go back to reference Avihingsanon Y, Benjachat T, Tassanarong A, Sodsai P, Kittikovit V, Hirankarn N (2009) Decreased renal expression of vascular endothelial growth factor in lupus nephritis is associated with worse prognosis. Kidney Int 75:1340–1348PubMedCrossRef Avihingsanon Y, Benjachat T, Tassanarong A, Sodsai P, Kittikovit V, Hirankarn N (2009) Decreased renal expression of vascular endothelial growth factor in lupus nephritis is associated with worse prognosis. Kidney Int 75:1340–1348PubMedCrossRef
91.
go back to reference Edelbauer M, Kshirsagar S, Riedl M, Billing H, Tonshoff B, Haffner D, Dotsch J, Wechselberger G, Weber LT, Steichen-Gersdorf E (2012) Soluble VEGF receptor 1 promotes endothelial injury in children and adolescents with lupus nephritis. Pediatr Nephrol 27:793–800. Edelbauer M, Kshirsagar S, Riedl M, Billing H, Tonshoff B, Haffner D, Dotsch J, Wechselberger G, Weber LT, Steichen-Gersdorf E (2012) Soluble VEGF receptor 1 promotes endothelial injury in children and adolescents with lupus nephritis. Pediatr Nephrol 27:793–800.
92.
go back to reference Dhaun N, Lilitkarntakul P, Macintyre IM, Muilwijk E, Johnston NR, Kluth DC, Webb DJ, Goddard J (2009) Urinary endothelin-1 in chronic kidney disease and as a marker of disease activity in lupus nephritis. Am J Physiol Renal Physiol 296:1477–1483CrossRef Dhaun N, Lilitkarntakul P, Macintyre IM, Muilwijk E, Johnston NR, Kluth DC, Webb DJ, Goddard J (2009) Urinary endothelin-1 in chronic kidney disease and as a marker of disease activity in lupus nephritis. Am J Physiol Renal Physiol 296:1477–1483CrossRef
93.
go back to reference Wang G, Lai FM, Tam LS, Li EK, Kwan BC, Chow KM, Li PK, Szeto CC (2009) Urinary FOXP3 mRNA in patients with lupus nephritis–relation with disease activity and treatment response. Rheumatology (Oxford) 48:755–760CrossRef Wang G, Lai FM, Tam LS, Li EK, Kwan BC, Chow KM, Li PK, Szeto CC (2009) Urinary FOXP3 mRNA in patients with lupus nephritis–relation with disease activity and treatment response. Rheumatology (Oxford) 48:755–760CrossRef
94.
go back to reference Brunner HI, Bennett MR, Mina R, Suzuki M, Petri M, Kiani AN, Pendl J, Witte D, Ying J, Rovin BH, Devarajan P (2012) Non-invasive renal protein biomarkers are associated with histological features of lupus nephritis. Arthritis Rheum. doi:10.1002/art.34426 Brunner HI, Bennett MR, Mina R, Suzuki M, Petri M, Kiani AN, Pendl J, Witte D, Ying J, Rovin BH, Devarajan P (2012) Non-invasive renal protein biomarkers are associated with histological features of lupus nephritis. Arthritis Rheum. doi:10.​1002/​art.​34426
Metadata
Title
Urine biomarkers in juvenile-onset SLE nephritis
Authors
Louise Watson
Michael W. Beresford
Publication date
01-03-2013
Publisher
Springer-Verlag
Published in
Pediatric Nephrology / Issue 3/2013
Print ISSN: 0931-041X
Electronic ISSN: 1432-198X
DOI
https://doi.org/10.1007/s00467-012-2184-y

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