Skip to main content

Lupus Nephritis (Including Antiphospholipid Antibody Syndrome), Pediatric

  • Living reference work entry
  • First Online:
Glomerulonephritis

Abstract

Childhood-onset systemic lupus erythematosus (cSLE) has been defined as a subset of SLE with onset prior to 18 years of age. Around 15% of SLE patients present with nephritis before this age, and debatably these patients have a greater genetic component to their disease etiology, a more systemic involvement, and a more severe disease course. Patients develop their loss of tolerance to self at an earlier time than patients with adult-onset SLE, or at least their loss of tolerance progresses sooner to immune complex deposition and tissue injury. In this chapter, we review the joint approach of pediatric nephrologists and rheumatologists towards patients with cSLE and nephritis. We address the areas where evidence exists and the areas where we must rely on expert opinion or evidence based on primarily adult studies. Fortunately, 5- and 10-year mortality is lower than in adult-onset lupus nephritis, and patient and renal survival has improved over the years. However, relapses during the transition from adolescence to adulthood are common and cardiovascular and infectious complications are frequent in long-term survivors.

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

Access this chapter

Institutional subscriptions

References

  • Alarcon GS, Mcgwin G Jr, Petri M, Reveille JD, Ramsey-Goldman R, Kimberly RP (2002) Baseline characteristics of a multiethnic lupus cohort: profile. Lupus 11:95–101

    Article  CAS  PubMed  Google Scholar 

  • Alarcon-Segovia D, Alarcon-Riquelme ME, Cardiel MH, Caeiro F, Massardo L, Villa AR, Pons-Estel BA (2005) Familial aggregation of systemic lupus erythematosus, rheumatoid arthritis, and other autoimmune diseases in 1,177 lupus patients from the gladel cohort. Arthritis Rheum 52:1138–1147

    Article  PubMed  Google Scholar 

  • Ambrose N, Morgan TA, Galloway J, Ionnoau Y, Beresford MW, Isenberg DA (2016) Differences in disease phenotype and severity in SLE across age groups. Lupus 25:1542–1550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Appel GB, Contreras G, Dooley MA, Ginzler EM, Isenberg D, Jayne D, Li LS, Mysler E, Sanchez-Guerrero J, Solomons N, Wofsy D (2009) Mycophenolate mofetil versus cyclophosphamide for induction treatment of lupus nephritis. J Am Soc Nephrol 20:1103–1112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aragon E, Resontoc LP, Chan YH, Lau YW, Tan PH, Loh HL, Ng KH, Yap HK (2016) Long-term outcomes with multi-targeted immunosuppressive protocol in children with severe proliferative lupus nephritis. Lupus 25:399–406

    Article  CAS  PubMed  Google Scholar 

  • Ardoin SP, Schanberg LE, Sandborg CI, Barnhart HX, Evans GW, Yow E, Mieszkalski KL, Ilowite NT, Eberhard A, Imundo LF, Kimura Y, Levy D, Von Scheven E, Silverman E, Bowyer SL, Punaro L, Singer NG, Sherry DD, Mccurdy DK, Klein-Gitelman M, Wallace C, Silver RM, Wagner-Weiner L, Higgins GC, Brunner HI, Jung L, Soep JB, Reed AM, Thompson SD (2014) Secondary analysis of APPLE study suggests atorvastatin may reduce atherosclerosis progression in pubertal lupus patients with higher C reactive protein. Ann Rheum Dis 73:557–566

    Article  CAS  PubMed  Google Scholar 

  • Aronoff G, Bennett W, Berns J (2007) Drug prescribing in renal failure: dosing guidelines for adults and children. American College Of Physicians, Philadelphia

    Google Scholar 

  • 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 22:981–986

    Article  PubMed  Google Scholar 

  • Austin HA 3rd, Muenz LR, Joyce KM, Antonovych TA, Kullick ME, Klippel JH, Decker JL, Balow JE (1983) Prognostic factors in lupus nephritis. contribution of renal histologic data. Am J Med 75:382–391

    Article  PubMed  Google Scholar 

  • Austin HA 3rd, Klippel JH, Balow JE, Le Riche NG, Steinberg AD, Plotz PH, Decker JL (1986) Therapy of lupus nephritis. Controlled trial of prednisone and cytotoxic drugs. N Engl J Med 314:614–619

    Article  PubMed  Google Scholar 

  • Avcin T, Cimaz R, Silverman ED, Cervera R, Gattorno M, Garay S, Berkun Y, Sztajnbok FR, Silva CA, Campos LM, Saad-Magalhaes C, Rigante D, Ravelli A, Martini A, Rozman B, Meroni PL (2008) Pediatric antiphospholipid syndrome: clinical and immunologic features of 121 patients in an international registry. Pediatrics 122:E1100–E1107

    Article  PubMed  Google Scholar 

  • Bao L, Haas M, Boackle SA, Kraus DM, Cunningham PN, Park P, Alexander JJ, Anderson RK, Culhane K, Holers VM, Quigg RJ (2002) Transgenic expression of a soluble complement inhibitor protects against renal disease and promotes survival in MRL/Lpr Mice. J Immunol 168(7):3601

    Article  CAS  PubMed  Google Scholar 

  • Baqi N, Moazami S, Singh A, Ahmad H, Balachandra S, Tejani A (1996) Lupus nephritis in children: a longitudinal study of prognostic factors and therapy. J Am Soc Nephrol 7:924–929

    CAS  PubMed  Google Scholar 

  • Barber CE, Geldenhuys L, Hanly JG (2006) Sustained remission of lupus nephritis. Lupus 15:94–101

    Article  CAS  PubMed  Google Scholar 

  • Barbhaiya M, Costenbader K (2014) Ultraviolet radiation and systemic lupus erythematosus. Lupus 23:588–595

    Article  CAS  PubMed  Google Scholar 

  • Bartosh SM, Fine RN, Sullivan EK (2001) Outcome after transplantation of young patients with systemic lupus erythematosus: a report of the North American pediatric renal transplant cooperative study. Transplantation 72:973–978

    Article  CAS  PubMed  Google Scholar 

  • Baskin E, Agras PI, Menekse N, Ozdemir H, Cengiz N (2007) Full-house nephropathy in a patient with negative serology for lupus. Rheumatol Int 27:281–284

    Article  PubMed  Google Scholar 

  • Batinić D, Milošević D, Čorić M, Topalović-Grković M, Jelušić M, Turudić D (2015) Lupus nephritis in croatian children: clinicopathologic findings and outcome. Lupus 24:307–314

    Article  PubMed  Google Scholar 

  • Beck LH Jr, Salant DJ (2009) Treatment of membranous lupus nephritis: where are we now? J Am Soc Nephrol 20:690–691

    Article  CAS  PubMed  Google Scholar 

  • Bergtold A, Gavhane A, D’Agati V, Madaio M, Clynes R (2006) FcR-bearing myeloid cells are responsible for triggering murine lupus nephritis. J Immunol 177:7287–7295

    Article  CAS  PubMed  Google Scholar 

  • Berkun Y, Padeh S, Barash J, Uziel Y, Harel L, Mukamel M, Revel-Vilk S, Kenet G (2006) Antiphospholipid syndrome and recurrent thrombosis in children. Arthritis Rheum 55:850–855

    Article  CAS  PubMed  Google Scholar 

  • Bernatsky S, Boivin JF, Joseph L, Manzi S, Ginzler E, Gladman DD, Urowitz M, Fortin PR, Petri M, Barr S, Gordon C, Bae SC, Isenberg D, Zoma A, Aranow C, Dooley MA, Nived O, Sturfelt G, Steinsson K, Alarcon G, Senecal JL, Zummer M, Hanly J, Ensworth S, Pope J, Edworthy S, Rahman A, Sibley J, El-Gabalawy H, Mccarthy T, St Pierre Y, Clarke A, Ramsey-Goldman R (2006) Mortality in systemic lupus erythematosus. Arthritis Rheum 54:2550–2557

    Article  CAS  PubMed  Google Scholar 

  • Berthier CC, Bethunaickan R, Gonzalez-Rivera T, Nair V, Ramanujam M, Zhang W, Bottinger EP, Segerer S, Lindenmeyer M, Cohen CD, Davidson A, Kretzler M (2012) Cross-species transcriptional network analysis defines shared inflammatory responses in murine and human lupus nephritis. J Immunol 189:988–1001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bethunaickan R, Sahu R, Liu Z, Tang YT, Huang W, Edegbe O, Tao H, Ramanujam M, Madaio MP, Davidson A (2012) Anti-tumor necrosis factor Α treatment of interferon-Α–induced murine lupus nephritis reduces the renal macrophage response but does not alter glomerular immune complex formation. Arthritis Rheumat 64:3399–3408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Block SR, Winfield JB, Lockshin MD, D’Angelo WA, Christian CL (1975) Studies of twins with systemic lupus erythematosus. A review of the literature and presentation of 12 additional sets. Am J Med 59:533–552

    Article  CAS  PubMed  Google Scholar 

  • Bogdanovic R, Nikolic V, Pasic S, Dimitrijevic J, Lipkovska-Markovic J, Eric-Marinkovic J, Ognjanovic M, Minic A, Stajic N (2004) Lupus nephritis in childhood: a review of 53 patients followed at a single center. Pediatr Nephrol 19:36–44

    Article  PubMed  Google Scholar 

  • Bomback AS, Markowitz GS (2016) Lupus podocytopathy: a distinct entity. Clin J Am Soc Nephrol 11:547–548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boneparth A, Davidson A (2012) B-cell activating factor targeted therapy and lupus. Arthritis Res Ther 14:S2

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Boneparth A, Ilowite N (2014) Comparison of renal response parameters for juvenile membranous plus proliferative lupus nephritis versus isolated proliferative lupus nephritis: a cross-sectional analysis of the CARRA Registry. Lupus 23:898–904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boneparth A, Wenderfer SE, Moorthy LN, Radhakrishna SM, Sagcal-Gironella AC, Von Scheven E (2016) Clinical characteristics of children with membranous lupus nephritis: the Childhood Arthritis and Rheumatology Research Alliance Legacy Registry. Lupus 26:299–306

    Article  PubMed  Google Scholar 

  • Boros CA, Bradley TJ, Cheung MM, Bargman JM, Russell JL, Mccrindle BW, Adeli K, Hamilton J, Silverman ED (2011) Early determinants of atherosclerosis in paediatric systemic lupus erythematosus. Clin Exp Rheumatol 29:575–581

    CAS  PubMed  Google Scholar 

  • Botto M, Dell’Agnola C, Bygrave AE, Thompson EM, Cook HT, Petry F, Loos M, Pandolfi PP, Walport MJ (1998) Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat Genet 19:56–59

    Article  CAS  PubMed  Google Scholar 

  • Broder A, Khattri S, Patel R, Putterman C (2011) Undertreatment of disease activity in systemic lupus erythematosus patients with endstage renal failure is associated with increased all-cause mortality. J Rheumatol 38:2382–2389

    Article  PubMed  PubMed Central  Google Scholar 

  • Bruce IN, Hallett DC, Gladman DD, Urowitz MB (1999) Extrarenal disease activity in systemic lupus erythematosus is not suppressed by chronic renal insufficiency or renal replacement therapy. J Rheumatol 26:1490–1494

    CAS  PubMed  Google Scholar 

  • 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 58:556–562

    Article  PubMed  Google Scholar 

  • Brunner HI, Silva CA, Reiff A, Higgins GC, Imundo L, Williams CB, Wallace CA, Aikawa NE, Nelson S, Klein-Gitelman MS, Rose SR (2015) Randomized double-blinded dose escalation trial of triptorelin for ovary protection in childhood-onset systemic lupus erythematosus. Arthritis Rheumatol 67:1377–1385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brunner HI, Bennett M, Abulaban K, Klein-Gitelman M, O’Neil K, Tucker L, Ardoin S, Rouster-Stevens K, Onel K, Singer N, Eberhard BA, Jung L, Imundo L, Wright T, Witte D, Rovin B, Ying J, Devarajan P (2016) Development of a novel renal activity index of lupus nephritis in children & young adults. Arthritis Care Res 68:1003–1011

    Article  CAS  Google Scholar 

  • Bruschi M, Sinico RA, Moroni G, Pratesi F, Migliorini P, Galetti M, Murtas C, Tincani A, Madaio M, Radice A, Franceschini F, Trezzi B, Bianchi L, Giallongo A, Gatti R, Tardanico R, Scaloni A, D’ambrosio C, Carnevali ML, Messa P, Ravani P, Barbano G, Bianco B, Bonanni A, Scolari F, Martini A, Candiano G, Allegri L, Ghiggeri GM (2014) Glomerular autoimmune multicomponents of human lupus nephritis in vivo: Α-enolase and annexin AI. J Am Soc Nephrol 25:2483–2498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bullo M, Tschumi S, Bucher BS, Bianchetti MG, Simonetti GD (2012) Pregnancy outcome following exposure to angiotensin-converting enzyme inhibitors or angiotensin receptor antagonists: a systematic review. Hypertension 60:444–450

    Article  CAS  PubMed  Google Scholar 

  • Buratti S, Szer IS, Spencer CH, Bartosh S, Reiff A (2001) Mycophenolate mofetil treatment of severe renal disease in pediatric onset systemic lupus erythematosus. J Rheumatol 28:2103–2108

    CAS  PubMed  Google Scholar 

  • Caeiro F, Michielson FM, Bernstein R, Hughes GR, Ansell BM (1981) Systemic lupus erythematosus in childhood. Ann Rheum Dis 40:325–31

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caltik A, Demircin G, Bulbul M, Erdogan O, Akyuz SG, Arda N (2013) An unusual case of ana negative systemic lupus erythematosus presented with vasculitis, long-standing serositis and full-house nephropathy. Rheumatol Int 33:219–222

    Article  PubMed  Google Scholar 

  • Cameron JS (1994) Lupus nephritis in childhood and adolescence. Pediatr Nephrol 8:230–249

    Article  CAS  PubMed  Google Scholar 

  • Campbell JF, Swartz SJ, Wenderfer SE (2015) Nocturnal hypertension and attenuated nocturnal blood pressure dipping is common in pediatric lupus. F1000Res 4:164

    PubMed  PubMed Central  Google Scholar 

  • Casella C, Seguro L, Takayama L, Medeiros D, Bonfa E, Pereira R (2012) Juvenile onset systemic lupus erythematosus: a possible role for vitamin D in disease status and bone health. Lupus 21:1335–1342

    Article  CAS  PubMed  Google Scholar 

  • Caster DJ, Korte EA, Nanda SK, Mcleish KR, Oliver RK, G’Sell RT, Sheehan RM, Freeman DW, Coventry SC, Kelly JA, Guthridge JM, James JA, Sivils KL, Alarcon-Riquelme ME, Scofield RH, Adrianto I, Gaffney PM, Stevens AM, Freedman BI, Langefeld CD, Tsao BP, Pons-Estel BA, Jacob CO, Kamen DL, Gilkeson GS, Brown EE, Alarcon GS, Edberg JC, Kimberly RP, Martin J, Merrill JT, Harley JB, Kaufman KM, Reveille JD, Anaya J-M, Criswell LA, Vila LM, Petri M, Ramsey-Goldman R, Bae S-C, Boackle SA, Vyse TJ, Niewold TB, Cohen P, Powell DW (2013) Abin1 dysfunction as a genetic basis for lupus nephritis. J Am Soc Nephrol 24:1743–1754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang A, Henderson SG, Brandt D, Liu N, Guttikonda R, Hsieh C, Kaverina N, Utset TO, Meehan SM, Quigg RJ, Meffre E, Clark MR (2011) In situ B cell-mediated immune responses and tubulointerstitial inflammation in human lupus nephritis. J Immunol 186:1849–1860

    Article  CAS  PubMed  Google Scholar 

  • Chang YS, Liu CJ, Wu TH, Chaou CH, Lin KC, Ou SM, Chen TJ, Chen WS, Chou CT, Tsai CY (2013) Survival analysis in systemic lupus erythematosus patients on maintenance dialysis: a nationwide population-based study in Taiwan. Rheumatology (Oxford) 52:166–172

    Article  Google Scholar 

  • Charles N, Hardwick D, Daugas E, Illei GG, Rivera J (2010) Basophils and the T helper 2 environment can promote the development of lupus nephritis. Nat Med 16:701–707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen W, Tang X, Liu Q, Fu P, Liu F, Liao Y, Yang Z, Zhang J, Chen J, Lou T, Fu J, Kong Y, Liu Z, Fan A, Rao S, Li Z, Yu X (2011) Short-term outcomes of induction therapy with tacrolimus versus cyclophosphamide for active lupus nephritis: a multicenter randomized clinical trial. Am J Kidney Dis 57:235–244

    Article  CAS  PubMed  Google Scholar 

  • Cheunsuchon B, Rungkaew P, Chawanasuntorapoj R, Pattaragarn A, Parichatikanond P (2007) Prevalence and clinicopathologic findings of antiphospholipid syndrome nephropathy in Thai systemic lupus erythematosus patients who underwent renal biopsies. Nephrology (Carlton) 12:474–480

    Article  Google Scholar 

  • Contis A, Vanquaethem H, Truchetet ME, Couzi L, Rigothier C, Richez C, Lazaro E, Duffau P (2016) Analysis of the effectiveness and safety of rituximab in patients with refractory lupus nephritis: a chart review. Clin Rheumatol 35:517–522

    Article  PubMed  Google Scholar 

  • Contreras G, Mattiazzi A, Guerra G, Ortega LM, Tozman EC, Li H, Tamariz L, Carvalho C, Kupin W, Ladino M, Leclercq B, Jaraba I, Carvalho D, Carles E, Roth D (2010) Recurrence of lupus nephritis after kidney transplantation. J Am Soc Nephrol 21(7):1200

    Article  PubMed  PubMed Central  Google Scholar 

  • Cornacchia E, Golbus J, Maybaum J, Strahler J, Hanash S, Richardson B (1988) Hydralazine and procainamide inhibit T cell DNA methylation and induce autoreactivity. J Immunol 140:2197–2200

    CAS  PubMed  Google Scholar 

  • Cramer CH 2nd, Mills M, Valentini RP, Smoyer WE, Haftel H, Brophy PD (2007) Clinical presentation and outcome in a cohort of paediatric patients with membranous lupus nephritis. Nephrol Dial Transplant 22:3495–3500

    Article  PubMed  Google Scholar 

  • Crispin JC, Oukka M, Bayliss G, Cohen RA, Van Beek CA, Stillman IE, Kyttaris VC, Juang YT, Tsokos GC (2008) Expanded double negative T cells in patients with systemic lupus erythematosus produce IL-17 and infiltrate the kidneys. J Immunol 181:8761–8766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • D’Cruz DP (2005) Renal manifestations of the antiphospholipid syndrome. Lupus 14:45–48

    Article  PubMed  Google Scholar 

  • Daehn I, Casalena G, Zhang T, Shi S, Fenninger F, Barasch N, Yu L, D’Agati V, Schlondorff D, Kriz W, Haraldsson B, Bottinger EP (2014) Endothelial mitochondrial oxidative stress determines podocyte depletion in segmental glomerulosclerosis. J Clin Invest 124:1608–1621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daleboudt GM, Bajema IM, Goemaere NN, Van Laar JM, Bruijn JA, Berger SP (2009) The clinical relevance of a repeat biopsy in lupus nephritis flares. Nephrol Dial Transplant 24(12):3712–3717

    Article  PubMed  Google Scholar 

  • Dang J, Shan S, Li J, Zhao H, Xin Q, Liu Y, Bian X, Liu Q (2014) Gene-gene interactions of IRF5, STAT4, IKZF1 and ETS1 in systemic lupus erythematosus. Tissue Antigens 83:401–408

    Article  CAS  PubMed  Google Scholar 

  • Deapen D, Escalante A, Weinrib L, Horwitz D, Bachman B, Roy-Burman P, Walker A, Mack TM (1992) A revised estimate of twin concordance in systemic lupus erythematosus. Arthritis Rheum 35:311–318

    Article  CAS  PubMed  Google Scholar 

  • Deocharan B, Qing X, Lichauco J, Putterman C (2002) Alpha-actinin is a cross-reactive renal target for pathogenic anti-DNA antibodies. J Immunol 168:3072–3078

    Article  CAS  PubMed  Google Scholar 

  • Dieker J, Tel J, Pieterse E, Thielen A, Rother N, Bakker M, Fransen J, Dijkman HB, Berden JH, De Vries JM, Hilbrands LB, Van Der Vlag J (2016) Circulating apoptotic microparticles in systemic lupus erythematosus patients drive the activation of dendritic cell subsets and prime neutrophils for netosis. Arthritis Rheumatol 68:462–472

    Article  CAS  PubMed  Google Scholar 

  • Dinu AR, Merrill JT, Shen C, Antonov IV, Myones BL, Lahita RG (1998) Frequency of antibodies to the cholesterol transport protein apolipoprotein A1 in patients with SLE. Lupus 7:355–360

    Article  CAS  PubMed  Google Scholar 

  • Dooley MA, Nair R (2008) Therapy insight: preserving fertility in cyclophosphamide-treated patients with rheumatic disease. Nat Clin Pract Rheumatol 4:250–257

    Article  CAS  PubMed  Google Scholar 

  • Duran-Barragan S, Mcgwin G Jr, Vila LM, Reveille JD, Alarcon GS (2008) Angiotensin-converting enzyme inhibitors delay the occurrence of renal involvement and are associated with a decreased risk of disease activity in patients with systemic lupus erythematosus – results from LUMINA (LIX): a multiethnic US cohort. Rheumatology (Oxford) 47:1093–1096

    Article  CAS  Google Scholar 

  • Eberhard A, Sparling C, Sudbury S, Ford P, Laxer R, Silverman E (1994) Hypoprothrombinemia in childhood systemic lupus erythematosus. Semin Arthritis Rheum 24:12–18

    Article  CAS  PubMed  Google Scholar 

  • Einav S, Pozdnyakova OO, Ma M, Carroll MC (2002) Complement C4 is protective for lupus disease independent of C3. J Immunol 168:1036–1041

    Article  CAS  PubMed  Google Scholar 

  • El Gamal YM, Elmasry OA, El Hadidi IS, Soliman OK (2013) Proximal aortic stiffness is increased in systemic lupus erythematosus activity in children and adolescents. ISRN Pediatr 2013:765253

    Article  PubMed  PubMed Central  Google Scholar 

  • El-Hewala A, Nageeb GS, El-Shahawy EE, Sharaf DM, Omran AA, El-Messallamy FAF, Eassa S (2011) Anti-C1q and anti-dsDNA antibodies in systemic lupus erythematosus: relationship with disease activity and renal involvement in Sharkia governorate, Egypt. Egypt Rheumatol 33:203–208

    Article  CAS  Google Scholar 

  • Enriquez JL, Rajaraman S, Kalia A, Brouhard BH, Travis LB (1988) Isolated antinuclear antibody-negative lupus nephropathy in young children. Child Nephrol Urol 9:340–346

    PubMed  Google Scholar 

  • Ettinger WH, Goldberg AP, Applebaum-Bowden D, Hazzard WR (1987) Dyslipoproteinemia in systemic lupus erythematosus effect of corticosteroids. Am J Med 83:503–508

    Article  CAS  PubMed  Google Scholar 

  • Falcini F, Capannini S, Martini G, La Torre F, Vitale A, Mangiantini F, Nacci F, Cerinic MM, Cimaz R, Zulian F (2009) Mycophenolate mofetil for the treatment of juvenile onset SLE: a multicenter study. Lupus 18:139–143

    Article  CAS  PubMed  Google Scholar 

  • Fessler BJ, Alarcon GS, Mcgwin G Jr, Roseman J, Bastian HM, Friedman AW, Baethge BA, Vila L, Reveille JD (2005) Systemic lupus erythematosus in three ethnic groups: XVI. Association of hydroxychloroquine use with reduced risk of damage accrual. Arthritis Rheum 52:1473–1480

    Article  PubMed  Google Scholar 

  • Fish AJ, Blau EB, Westberg NG, Burke BA, Vernier RL, Michael AF (1977) Systemic lupus erythematosus within the first two decades of life. Am J Med 62:99–117

    Article  CAS  PubMed  Google Scholar 

  • Freedman BI, Langefeld CD, Andringa KK, Croker JA, Williams AH, Garner NE, Birmingham DJ, Hebert LA, Hicks PJ, Segal MS, Edberg JC, Brown EE, Alarcon GS, Costenbader KH, Comeau ME, Criswell LA, Harley JB, James JA, Kamen DL, Lim SS, Merrill JT, Sivils KL, Niewold TB, Patel NM, Petri M, Ramsey-Goldman R, Reveille JD, Salmon JE, Tsao BP, Gibson KL, Byers JR, Vinnikova AK, Lea JP, Julian BA, Kimberly RP, On Behalf of the Lupus Nephritis– E. C (2014) End-stage kidney disease in African Americans with lupus nephritis associates with Apol1. Arthritis Rheumatol 66:390–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu LW, Yang LY, Chen WP, Lin CY (1998) Clinical efficacy of cyclosporin a neoral in the treatment of paediatric lupus nephritis with heavy proteinuria. Br J Rheumatol 37:217–221

    Article  CAS  PubMed  Google Scholar 

  • Fukuyama H, Nimmerjahn F, Ravetch JV (2004) The inhibitory Fcγ receptor modulates autoimmunity by limiting the accumulation of immunoglobulin G+ anti-DNA plasma cells. Nat Immunol 6:99–106

    Article  PubMed  CAS  Google Scholar 

  • Gajjar R, Miller SD, Meyers KE, Ginsberg JP (2015) Fertility preservation in patients receiving cyclophosphamide therapy for renal disease. Pediatr Nephrol 30:1099–1106

    Article  PubMed  Google Scholar 

  • Gateva V, Sandling JK, Hom G, Taylor KE, Chung SA, Sun X, Ortmann W, Kosoy R, Ferreira RC, Nordmark G, Gunnarsson I, Svenungsson E, Padyukov L, Sturfelt G, Jonsen A, Bengtsson AA, Rantapaa-Dahlqvist S, Baechler EC, Brown EE, Alarcon GS, Edberg JC, Ramsey-Goldman R, Mcgwin G Jr, Reveille JD, Vila LM, Kimberly RP, Manzi S, Petri MA, Lee A, Gregersen PK, Seldin MF, Ronnblom L, Criswell LA, Syvanen AC, Behrens TW, Graham RR (2009) A large-scale replication study identifies Tnip1, PRDM1, JAZF1, UHRF1BP1 and IL10 as risk loci for systemic lupus erythematosus. Nat Genet 41:1228–1233

    Google Scholar 

  • Getts DR, Chastain EML, Terry RL, Miller SD (2013) Virus infection, antiviral immunity, and autoimmunity. Immunol Rev 255:197–209

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gianviti A, Barsotti P, Barbera V, Faraggiana T, Rizzoni G (1999) Delayed onset of systemic lupus erythematosus in patients with “full-house” nephropathy. Pediatr Nephrol 13:683–687

    Article  CAS  PubMed  Google Scholar 

  • Gibson KL, Gipson DS, Massengill SA, Dooley MA, Primack WA, Ferris MA, Hogan SL (2009) Predictors of relapse and end stage kidney disease in proliferative lupus nephritis: focus on children, adolescents, and young adults. Clin J Am Soc Nephrol 4:1962–1967

    Article  PubMed  PubMed Central  Google Scholar 

  • Gilkeson GS, Mashmoushi AK, Ruiz P, Caza TN, Perl A, Oates JC (2013) Endothelial nitric oxide synthase reduces crescentic and necrotic glomerular lesions, reactive oxygen production, and MCP1 production in murine lupus nephritis. PLoS One 8:E64650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glidden RS, Mantzouranis EC, Borel Y (1983) Systemic lupus erythematosus in childhood: clinical manifestations and improved survival in fifty-five patients. Clin Immunol Immunopathol 29:196–210

    Article  CAS  PubMed  Google Scholar 

  • Gomez-Guerrero C, Lopez-Armada MJ, Gonzalez E, Egido J (1994) Soluble IgA and IgG aggregates are catabolized by cultured rat mesangial cells and induce production of TNF-alpha and IL-6, and proliferation. J Immunol 153:5247–5255

    CAS  PubMed  Google Scholar 

  • Gonzalez-Juanatey C, Llorca J, Vazquez-Rodriguez TR, Diaz-Varela N, Garcia-Quiroga H, Gonzalez-Gay MA (2008) Short-term improvement of endothelial function in rituximab-treated rheumatoid arthritis patients refractory to tumor necrosis factor alpha blocker therapy. Arthritis Rheum 59:1821–1824

    Article  CAS  PubMed  Google Scholar 

  • Goo YS, Park HC, Choi HY, Kim BS, Park YB, Lee SK, Kang SW, Kim SI, Kim YS, Park KI, Lee HY, Han DS, Choi KH (2004) The evolution of lupus activity among patients with end-stage renal disease secondary to lupus nephritis. Yonsei Med J 45:199–206

    Article  PubMed  Google Scholar 

  • Gordon C, Jayne D, Pusey C, Adu D, Amoura Z, Aringer M, Ballerin J, Cervera R, Calvo-Alen J, Chizzolini C, Dayer J, Doria A, Ferrario F, Floege J, Guillevin L, Haubitz M, Hiepe F, Houssiau F, Lesavre P, Lightstone L, Meroni P, Meyer O, Moulin B, O’Reilly K, Praga M, Schulze-Koops H, Sinico R, Smith K, Tincani A, Vasconcelos C, Hughes G (2009) European consensus statement on the terminology used in the management of lupus glomerulonephritis. Lupus 18:257–263

    Article  CAS  PubMed  Google Scholar 

  • Grishman E, Venkataseshan VS (1988) Vascular lesions in lupus nephritis. Mod Pathol 1:235–241

    CAS  PubMed  Google Scholar 

  • Gutierrez-Suarez R, Ruperto N, Gastaldi R, Pistorio A, Felici E, Burgos-Vargas R, Martini A, Ravelli A (2006) A Proposal for a pediatric version of the systemic lupus International Collaborating Clinics/American College Of Rheumatology Damage Index based on the analysis of 1,015 patients with juvenile-onset systemic lupus erythematosus. Arthritis Rheum 54:2989–2996

    Article  PubMed  Google Scholar 

  • 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 29:2635–2642

    PubMed  Google Scholar 

  • Hagge WW, Burke EC, Stickler GB (1967) Treatment of systemic lupus erythematosus complicated by nephritis in children. Pediatrics 40:822–827

    CAS  PubMed  Google Scholar 

  • Harley JB, Alarcon-Riquelme ME, Criswell LA, Jacob CO, Kimberly RP, Moser KL, Tsao BP, Vyse TJ, Langefeld CD, Nath SK, Guthridge JM, Cobb BL, Mirel DB, Marion MC, Williams AH, Divers J, Wang W, Frank SG, Namjou B, Gabriel SB, Lee AT, Gregersen PK, Behrens TW, Taylor KE, Fernando M, Zidovetzki R, Gaffney PM, Edberg JC, Rioux JD, Ojwang JO, James JA, Merrill JT, Gilkeson GS, Seldin MF, Yin H, Baechler EC, Li QZ, Wakeland EK, Bruner GR, Kaufman KM, Kelly JA (2008) Genome-wide association scan in women with systemic lupus erythematosus identifies susceptibility variants in ITGAM, PXK, KIAA1542 and other loci. Nat Genet 40:204–210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haywood ME, Rogers NJ, Rose SJ, Boyle J, Mcdermott A, Rankin JM, Thiruudaian V, Lewis MR, Fossati-Jimack L, Izui S, Walport MJ, Morley BJ (2004) Dissection of BXSB lupus phenotype using mice congenic for chromosome 1 demonstrates that separate intervals direct different aspects of disease. J Immunol 173:4277–4285

    Article  CAS  PubMed  Google Scholar 

  • Hersh AO, Trupin L, Yazdany J, Panopalis P, Julian L, Katz P, Criswell LA, Yelin E (2010) Childhoodonset disease as a predictor of mortality in an adult cohort of patients with systemic lupus erythematosus. Arthritis Care Res 62:1152–9

    Article  Google Scholar 

  • Hill GS, Delahousse M, Nochy D, Tomkiewicz E, Remy P, Mignon F, Mery JP (2000) A new morphologic index for the evaluation of renal biopsies in lupus nephritis. Kidney Int 58:1160–1173

    Article  CAS  PubMed  Google Scholar 

  • Hill GS, Delahousse M, Nochy D, Bariety J (2005) Class IV-S versus class IV-G lupus nephritis: clinical and morphologic differences suggesting different pathogenesis. Kidney Int 68:2288–2297

    Article  PubMed  Google Scholar 

  • Hiraki LT, Hamilton J, Silverman ED (2007) Measuring permanent damage in pediatric systemic lupus erythematosus. Lupus 16:657–662

    Article  CAS  PubMed  Google Scholar 

  • Hiraki LT, Benseler SM, Tyrrell PN, Hebert D, Harvey E, Silverman ED (2008) Clinical and laboratory characteristics and long-term outcome of pediatric systemic lupus erythematosus: a longitudinal study. J Pediatr 152:550–556

    Article  PubMed  Google Scholar 

  • 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 63:1988–1997

    Article  PubMed  PubMed Central  Google Scholar 

  • Hiraki LT, Feldman CH, Liu J, Alarcón GS, Fischer MA, Winkelmayer WC, Costenbader KH (2012) Prevalence, incidence, and demographics of systemic lupus erythematosus and lupus nephritis from 2000 to 2004 among children in the US medicaid beneficiary population. Arthritis Rheum 64:2669–2676

    Article  PubMed  PubMed Central  Google Scholar 

  • Ho JC, Ahn C, Lim CS, Chung HK et al (2000) Clinical implications of antineutrophil cytoplasmic antibody test in lupus nephritis. Am J Nephrol 20:57–63

    Article  Google Scholar 

  • Hochberg MC (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 40:1725

    Article  CAS  PubMed  Google Scholar 

  • Houssiau FA, Vasconcelos C, D’Cruz D, Sebastiani GD, Garrido Ed Ede R, Danieli MG, Abramovicz D, Blockmans D, Mathieu A, Direskeneli H, Galeazzi M, Gul A, Levy Y, Petera P, Popovic R, Petrovic R, Sinico RA, Cattaneo R, Font J, Depresseux G, Cosyns JP, Cervera R (2002) Immunosuppressive therapy in lupus nephritis: the euro-lupus nephritis trial, a randomized trial of low-dose versus high-dose intravenous cyclophosphamide. Arthritis Rheum 46:2121–2131

    Article  CAS  PubMed  Google Scholar 

  • Houssiau FA, D’Cruz D, Sangle S, Remy P, Vasconcelos C, Petrovic R, Fiehn C, De Ramon Garrido E, Gilboe IM, Tektonidou M, Blockmans D, Ravelingien I, Le Guern V, Depresseux G, Guillevin L, Cervera R (2010a) Azathioprine versus mycophenolate mofetil for long-term immunosuppression in lupus nephritis: results from the maintain nephritis trial. Ann Rheum Dis 69:2083–2089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Houssiau FA, Vasconcelos C, D’Cruz D, Sebastiani GD, De Ramon Garrido E, Danieli MG, Abramovicz D, Blockmans D, Cauli A, Direskeneli H, Galeazzi M, Gul A, Levy Y, Petera P, Popovic R, Petrovic R, Sinico RA, Cattaneo R, Font J, Depresseux G, Cosyns JP, Cervera R (2010b) The 10-year follow-up data of the euro-lupus nephritis trial comparing low-dose and high-dose intravenous cyclophosphamide. Ann Rheum Dis 69:61–64

    Article  CAS  PubMed  Google Scholar 

  • Hu WX, Chen YH, Bao H, Liu ZZ, Wang SF, Zhang HT, Liu ZH (2015) Glucocorticoid with or without additional immunosuppressant therapy for patients with lupus podocytopathy: a retrospective single-center study. Lupus 24:1067–1075

    Article  CAS  PubMed  Google Scholar 

  • Hu W, Chen Y, Wang S, Chen H, Liu Z, Zeng C, Zhang H, Liu Z (2016) Clinical–morphological features and outcomes of lupus podocytopathy. Clin J Am Soc Nephrol 11:585–592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huerta A, Bomback AS, Liakopoulos V, Palanisamy A, D’Agati VV, Radhakrishnan J, Markowitz GS, Appel GB (2011) Renal-limited ‘lupus-like’ nephritis. Nephrol Dial Transplant 27:2337–2342

    Article  PubMed  CAS  Google Scholar 

  • Hugle B, Silverman E, Tyrrell P, Harvey E, Hébert D, Benseler S (2014) Presentation and outcome of paediatric membranous non-proliferative lupus nephritis. Pediatr Nephrol 30:113–121

    Article  PubMed  Google Scholar 

  • Ichii O, Konno A, Sasaki N, Endoh D, Hashimoto Y, Kon Y (2008) Autoimmune glomerulonephritis induced in congenic mouse strain carrying telomeric region of chromosome 1 derived from MRL/MpJ. Histol Histopathol 23:411–422

    CAS  PubMed  Google Scholar 

  • Ieko M, Sawada KI, Koike T, Notoya A, Mukai M, Kohno M, Wada N, Itoh T, Yoshioka N (1999) The putative mechanism of thrombosis in antiphospholipid syndrome: impairment of the protein C and the fibrinolytic systems by monoclonal anticardiolipin antibodies. Semin Thromb Hemost 25:503–507

    Article  CAS  PubMed  Google Scholar 

  • Ilowite NT, Samuel P, Ginzler E, Jacobson MS (1988) Dyslipoproteinemia in pediatric systemic lupus erythematosus. Arthritis Rheum 31:859–863

    Article  CAS  PubMed  Google Scholar 

  • Jarrot PA, Chiche L, Hervier B, Daniel L, Vuiblet V, Bardin N, Bertin D, Terrier B, Amoura Z, Andres E, Rondeau E, Hamidou M, Pennaforte JL, Halfon P, Daugas E, Dussol B, Puechal X, Kaplanski G, Jourde-Chiche N (2016) Systemic lupus erythematosus and antineutrophil cytoplasmic antibody-associated vasculitis overlap syndrome in patients with biopsy-proven glomerulonephritis. Medicine (Baltimore) 95:E3748

    Article  CAS  Google Scholar 

  • Jennette JC, Hipp CG (1985) Immunohistopathologic evaluation of C1q in 800 renal biopsy specimens. Am J Clin Pathol 83:415–420

    Article  CAS  PubMed  Google Scholar 

  • Kalaaji M, Fenton KA, Mortensen ES, Olsen R, Sturfelt G, Alm P, Rekvig OP (2007) Glomerular apoptotic nucleosomes are central target structures for nephritogenic antibodies in human SLE nephritis. Kidney Int 71:664–672

    Article  CAS  PubMed  Google Scholar 

  • Kallen RJ, Lee SK, Aronson AJ, Spargo BH (1977) Idiopathic membranous glomerulopathy preceding the emergence of systemic lupus erythematosus in two children. J Pediatr 90:72–76

    Article  CAS  PubMed  Google Scholar 

  • Kanda H, Kubo K, Tateishi S, Sato K, Yonezumi A, Yamamoto K, Mimura T (2005) Antiproteinuric effect of Arb in lupus nephritis patients with persistent proteinuria despite immunosuppressive therapy. Lupus 14:288–292

    Article  CAS  PubMed  Google Scholar 

  • Kang SH, Chung BH, Choi SR, Lee JY, Park HS, Sun IO, Choi BS, Park CW, Kim YS, Yang CW (2011) Comparison of clinical outcomes by different renal replacement therapy in patients with end-stage renal disease secondary to lupus nephritis. Korean J Intern Med 26:60–67

    Article  PubMed  PubMed Central  Google Scholar 

  • Kariuki SN, Franek BS, Kumar AA, Arrington J, Mikolaitis RA, Utset TO, Jolly M, Crow MK, Skol AD, Niewold TB (2010) Trait-stratified genome-wide association study identifies novel and diverse genetic associations with serologic and cytokine phenotypes in systemic lupus erythematosus. Arthritis Res Ther 12:R151

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kasitanon N, Fine DM, Haas M, Magder LS, Petri M (2006) Hydroxychloroquine use predicts complete renal remission within 12 months among patients treated with mycophenolate mofetil therapy for membranous lupus nephritis. Lupus 15:366–370

    Article  CAS  PubMed  Google Scholar 

  • Kdigo Working Group, T (2013) Pharmacological cholesterol-lowering treatment in children (chapter 4). Kidney Int Suppl 3:280–281

    Article  Google Scholar 

  • Khamashta MA, Cuadrado MJ, Mujic F, Taub NA, Hunt BJ, Hughes GR (1995) The management of thrombosis in the antiphospholipid-antibody syndrome. N Engl J Med 332:993–997

    Article  CAS  PubMed  Google Scholar 

  • Kidney Disease: Improving Global Outcomes (KDIGO) Glomerulonephritis Work Group, T (2012) Kdigo clinical practice guideline for glomerulonephritis. Kidney Int Suppl 2:139–274

    Article  Google Scholar 

  • Kinloch AJ, Chang A, Ko K, Henry Dunand CJ, Henderson S, Maienschein-Cline M, Kaverina N, Rovin BH, Salgado Ferrer M, Wolfgeher D, Liarski V, Haddon DJ, Utz PJ, Wilson PC, Clark MR (2014) Vimentin is a dominant target of in situ humoral immunity in human lupus tubulointerstitial nephritis. Arthritis Rheumatol 66:3359–3370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kitamura N, Matsukawa Y, Takei M, Sawada S (2009) Antiproteinuric effect of angiotensin-converting enzyme inhibitors and an angiotensin II receptor blocker in patients with lupus nephritis. J Int Med Res 37:892–898

    Article  CAS  PubMed  Google Scholar 

  • Kizawa T, Nozawa T, Kikuchi M, Nagahama K, Okudela K, Miyamae T, Imagawa T, Nakamura T, Mori M, Yokota S, Tsutsumi H (2014) Mycophenolate mofetil as maintenance therapy for childhood-onset systemic lupus erythematosus patients with severe lupus nephritis. Mod Rheumatol 25:210–214

    Article  PubMed  CAS  Google Scholar 

  • Kool M, Van Loo G, Waelput W, De Prijck S, Muskens F, Sze M, Van Praet J, Branco-Madeira F, Janssens S, Reizis B, Elewaut D, Beyaert R, Hammad H, Lambrecht BN (2011) The ubiquitin-editing protein A20 prevents dendritic cell activation, recognition of apoptotic cells, and systemic autoimmunity. Immunity 35:82–96

    Article  CAS  PubMed  Google Scholar 

  • Kraft SW, Schwartz MM, Korbet SM, Lewis EJ (2005) Glomerular podocytopathy in patients with systemic lupus erythematosus. J Am Soc Nephrol 16:175–179

    Article  PubMed  Google Scholar 

  • Krishnan MR, Wang C, Marion TN (2012) Anti-DNA autoantibodies initiate experimental lupus nephritis by binding directly to the glomerular basement membrane in mice. Kidney Int 82:184–192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumpers P, David S, Haubitz M, Hellpap J, Horn R, Brocker V, Schiffer M, Haller H, Witte T (2009) The Tie2 receptor antagonist angiopoietin 2 facilitates vascular inflammation in systemic lupus erythematosus. Ann Rheum Dis 68:1638–1643

    Article  CAS  PubMed  Google Scholar 

  • Kunz R, Friedrich C, Wolbers M, Mann JF (2008) Meta-analysis: effect of monotherapy and combination therapy with inhibitors of the renin angiotensin system on proteinuria in renal disease. Ann Intern Med 148:30–48

    Article  PubMed  Google Scholar 

  • Lateef A, Petri M (2013) Managing lupus patients during pregnancy. Best Pract Res Clin Rheumatol 27:435–447

    Article  PubMed  Google Scholar 

  • Lau KK, Jones DP, Ault BH (2007) Prognosis of lupus membranous nephritis in children. Lupus 16:70

    Article  CAS  PubMed  Google Scholar 

  • Lau KK, Ault BH, Jones DP, Butani L (2008) Induction therapy for pediatric focal proliferative lupus nephritis: cyclophosphamide versus mycophenolate mofetil. J Pediatr Health Care 22:282–288

    Article  PubMed  Google Scholar 

  • Lawman S, Mauri C, Jury EC, Cook HT, Ehrenstein MR (2004) Atorvastatin inhibits autoreactive B cell activation and delays lupus development in New Zealand Black/White F1 mice. J Immunol 173:7641–7646

    Article  CAS  PubMed  Google Scholar 

  • Leadbetter EA, Rifkin IR, Hohlbaum AM, Beaudette BC, Shlomchik MJ, Marshak-Rothstein A (2002) Chromatin-IgG complexes activate B cells by dual engagement of IgM and toll-like receptors. Nature 416:603–607

    Article  CAS  PubMed  Google Scholar 

  • Lee SJ, Schover LR, Partridge AH, Patrizio P, Wallace WH, Hagerty K, Beck LN, Brennan LV, Oktay K (2006) American Society of clinical oncology recommendations on fertility preservation in cancer patients. J Clin Oncol 24:2917–2931

    Article  PubMed  Google Scholar 

  • Lee BS, Cho HY, Kim EJ, Kang HG, Ha IS, Cheong HI, Kim JG, Lee HS, Choi Y (2007) Clinical outcomes of childhood lupus nephritis: a single center’s experience. Pediatr Nephrol 22:222–231

    Article  PubMed  Google Scholar 

  • Lee PY, Yeh KW, Yao TC, Lee WI, Lin YJ, Huang JL (2013) The outcome of patients with renal involvement in pediatric-onset systemic lupus erythematosus – a 20-year experience in Asia. Lupus 22:1534–1540

    Article  PubMed  Google Scholar 

  • Lehman TJ, Singh C, Ramanathan A, Alperin R, Adams A, Barinstein L, Moorthy N (2014) Prolonged improvement of childhood onset systemic lupus erythematosus following systematic administration of rituximab and cyclophosphamide. Pediatr Rheumatol 12:3

    Article  Google Scholar 

  • Levy DM, Kamphuis S (2012) Systemic lupus erythematosus in children and adolescents. Pediatr Clin N Am 59:345–364

    Article  Google Scholar 

  • Levy Y, Sherer Y, George J, Rovensky J, Lukac J, Rauova L, Poprac P, Langevitz P, Fabbrizzi F, Shoenfeld Y (2000) Intravenous immunoglobulin treatment of lupus nephritis. Semin Arthritis Rheum 29:321–327

    Article  CAS  PubMed  Google Scholar 

  • Li J, Liu Y, Xie C, Zhu J, Kreska D, Morel L, Mohan C (2005) Deficiency of type I interferon contributes to SLE2-associated component lupus phenotypes. Arthritis Rheum 52:3063–3072

    Article  CAS  PubMed  Google Scholar 

  • Liang MH, Schur PH, Fortin P, St. Clair EW, Balow JE, Costenbader K, Crofford L, Pablo PD, Dooley MA, Finckh A, Gordon CP, Lundberg IE, Meyrier A, Nived O, Ponticelli C, Schneider MK, Singh A, Wallace DJ (2006) The American College of Rheumatology response criteria for proliferative and membranous renal disease in systemic lupus erythematosus clinical trials. Arthritis Rheum 54:421–432

    Article  Google Scholar 

  • Lilleby V, Lien G, Frey Froslie K, Haugen M, Flato B, Forre O (2005) Frequency of osteopenia in children and young adults with childhood-onset systemic lupus erythematosus. Arthritis Rheum 52:2051–2059

    Article  PubMed  Google Scholar 

  • Lin CP, Adrianto I, Lessard CJ, Kelly JA, Kaufman KM, Guthridge JM, Freedman BI, Anaya JM, Alarcon-Riquelme ME, Pons-Estel BA, Martin J, Glenn S, Adler A, Bae SC, Park SY, Bang SY, Song YW, Boackle SA, Brown EE, Edberg JC, Alarcon GS, Petri MA, Criswell LA, Ramsey-Goldman R, Reveille JD, Vila LM, Gilkeson GS, Kamen DL, Ziegler J, Jacob CO, Rasmussen A, James JA, Kimberly RP, Merrill JT, Niewold TB, Scofield RH, Stevens AM, Tsao BP, Vyse TJ, Langefeld CD, Moser KL, Harley JB, Gaffney PM, Montgomery CG (2012) Role of Myh9 and Apol1 in African and non-African populations with lupus nephritis. Genes Immun 13:232–238

    Article  CAS  PubMed  Google Scholar 

  • Liu K, Li QZ, Delgado-Vega AM, Abelson AK, Sanchez E, Kelly JA, Li L, Liu Y, Zhou J, Yan M, Ye Q, Liu S, Xie C, Zhou XJ, Chung SA, Pons-Estel B, Witte T, De Ramon E, Bae SC, Barizzone N, Sebastiani GD, Merrill JT, Gregersen PK, Gilkeson GG, Kimberly RP, Vyse TJ, Kim I, D’Alfonso S, Martin J, Harley JB, Criswell LA, Wakeland EK, Alarcon-Riquelme ME, Mohan C (2009) Kallikrein genes are associated with lupus and glomerular basement membrane-specific antibody-induced nephritis in mice and humans. J Clin Invest 119:911–923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Zhang H, Liu Z, Xing C, Fu P, Ni Z, Chen J, Lin H, Liu F, He Y, He Y, Miao L, Chen N, Li Y, Gu Y, Shi W, Hu W, Liu Z, Bao H, Zeng C, Zhou M (2015) Multitarget therapy for induction treatment of lupus nephritis: a randomized trial. Ann Intern Med 162:18–26

    Article  PubMed  Google Scholar 

  • Livingston B, Bonner A, Pope J (2011) Differences in clinical manifestations between childhood-onset lupus and adult-onset lupus: a meta-analysis. Lupus 20:1345–1355

    Article  CAS  PubMed  Google Scholar 

  • Lood C, Blanco LP, Purmalek MM, Carmona-Rivera C, De Ravin SS, Smith CK, Malech HL, Ledbetter JA, Elkon KB, Kaplan MJ (2016) Neutrophil extracellular traps enriched in oxidized mitochondrial DNA are interferogenic and contribute to lupus-like disease. Nat Med 22:146–153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lozovoy MA, Simao AN, Morimoto HK, Iryioda TM, Panis C, Reiche EM, Borelli SD, Oliveira SR, Cecchini R, Dichi I (2014) Hypertension is associated with serologically active disease in patients with systemic lupus erythematosus: role of increased Th1/Th2 ratio and oxidative stress. Scand J Rheumatol 43:59–62

    Article  CAS  PubMed  Google Scholar 

  • Markle JGM, Frank DN, Mortin-Toth S, Robertson CE, Feazel LM, Rolle-Kampczyk U, Von Bergen M, Mccoy KD, Macpherson AJ, Danska JS (2013) Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 339:1084–1088

    Article  CAS  PubMed  Google Scholar 

  • Marks SD, Sebire NJ, Pilkington C, Tullus K (2007) Clinicopathological correlations of paediatric lupus nephritis. Pediatr Nephrol 22:77–83

    Article  PubMed  Google Scholar 

  • Maroz N, Segal MS (2013) Lupus nephritis and end-stage kidney disease. Am J Med Sci 346:319–323

    Article  PubMed  Google Scholar 

  • Marshall S, Dressler R, D’Agati V (1997) Membranous lupus nephritis with antineutrophil cytoplasmic antibody-associated segmental necrotizing and crescentic glomerulonephritis. Am J Kidney Dis 29:119–124

    Article  CAS  PubMed  Google Scholar 

  • Mccurdy DK, Lehman TJ, Bernstein B, Hanson V, King KK, Nadorra R, Landing BH (1992) Lupus nephritis: prognostic factors in children. Pediatrics 89:240–246

    CAS  PubMed  Google Scholar 

  • Mcmahon M, Grossman J, Skaggs B, Fitzgerald J, Sahakian L, Ragavendra N, Charles-Schoeman C, Watson K, Wong WK, Volkmann E, Chen W, Gorn A, Karpouzas G, Weisman M, Wallace DJ, Hahn BH (2009) Dysfunctional proinflammatory high-density lipoproteins confer increased risk of atherosclerosis in women with systemic lupus erythematosus. Arthritis Rheum 60:2428–2437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mcmahon M, Skaggs BJ, Sahakian L, Grossman J, Fitzgerald J, Ragavendra N, Charles-Schoeman C, Chernishof M, Gorn A, Witztum JL, Wong WK, Weisman M, Wallace DJ, La Cava A, Hahn BH (2011) High plasma leptin levels confer increased risk of atherosclerosis in women with systemic lupus erythematosus, and are associated with inflammatory oxidised lipids. Ann Rheum Dis 70:1619–1624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meislin AG, Rothfield N (1968) Systemic lupus erythematosus in childhood. Analysis of 42 cases, with comparative data on 200 adult cases followed concurrently. Pediatrics 42:37–49

    CAS  PubMed  Google Scholar 

  • Meistrich ML, Wilson G, Brown BW, Da Cunha MF, Lipshultz LI (1992) Impact of cyclophosphamide on long-term reduction in sperm count in men treated with combination chemotherapy for Ewing and soft tissue sarcomas. Cancer 70:2703–2712

    Article  CAS  PubMed  Google Scholar 

  • Menard L, Saadoun D, Isnardi I, Ng YS, Meyers G, Massad C, Price C, Abraham C, Motaghedi R, Buckner JH, Gregersen PK, Meffre E (2011) The PTPN22 allele encoding an R620w variant interferes with the removal of developing autoreactive B cells in humans. J Clin Invest 121:3635–3644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Midgley A, Beresford MW (2016) Increased expression of low density granulocytes in juvenile-onset systemic lupus erythematosus patients correlates with disease activity. Lupus 25:407–411

    Article  CAS  PubMed  Google Scholar 

  • Migliorini P, Baldini C, Rocchi V, Bombardieri S (2005) Anti-Sm and anti-RNP antibodies. Autoimmunity 38:47–54

    Article  CAS  PubMed  Google Scholar 

  • Migliorini A, Angelotti ML, Mulay SR, Kulkarni OO, Demleitner J, Dietrich A, Sagrinati C, Ballerini L, Peired A, Shankland SJ, Liapis H, Romagnani P, Anders HJ (2013) The antiviral cytokines IFN-alpha and IFN-beta modulate parietal epithelial cells and promote podocyte loss: implications for IFN toxicity, viral glomerulonephritis, and glomerular regeneration. Am J Pathol 183:431–440

    Article  CAS  PubMed  Google Scholar 

  • 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 64:375–383

    Article  Google Scholar 

  • Mok CC, Wong CK, To CH, Lai JP, Lam CS (2011) Effects of rosuvastatin on vascular biomarkers and carotid atherosclerosis in lupus: a randomized, double-blind, placebo-controlled trial. Arthritis Care Res (Hoboken) 63:875–883

    Article  CAS  Google Scholar 

  • Moorthy LN, Peterson MG, Hassett A, Baratelli M, Lehman TJ (2010) Impact of lupus on school attendance and performance. Lupus 19:620–627

    Article  CAS  PubMed  Google Scholar 

  • Morel L, Blenman KR, Croker BP, Wakeland EK (2001) The major murine systemic lupus erythematosus susceptibility locus, SLE1, is a cluster of functionally related genes. Proc Natl Acad Sci U S A 98:1787–1792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 37:490–498

    Article  CAS  PubMed  Google Scholar 

  • Mostoslavsky G, Fischel R, Yachimovich N, Yarkoni Y, Rosenmann E, Monestier M, Baniyash M, Eilat D (2001) Lupus anti-DNA autoantibodies cross-react with a glomerular structural protein: a case for tissue injury by molecular mimicry. Eur J Immunol 31:1221–1227

    Article  CAS  PubMed  Google Scholar 

  • Musone SL, Taylor KE, Lu TT, Nititham J, Ferreira RC, Ortmann W, Shifrin N, Petri MA, Kamboh MI, Manzi S, Seldin MF, Gregersen PK, Behrens TW, Ma A, Kwok PY, Criswell LA (2008) Multiple polymorphisms in the TNFAIP3 region are independently associated with systemic lupus erythematosus. Nat Genet 40:1062–1064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nasr SH, D’Agati VD, Park HR, Sterman PL, Goyzueta JD, Dressler RM, Hazlett SM, Pursell RN, Caputo C, Markowitz GS (2008) Necrotizing and crescentic lupus nephritis with antineutrophil cytoplasmic antibody seropositivity. Clin J Am Soc Nephrol 3:682–690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nasr R, Johns C, Gertner E (2014) Collapsing glomerulopathy in collagen vascular-like disease. Lupus 23:75–80

    Article  CAS  PubMed  Google Scholar 

  • Nathanson S, Salomon R, Ranchin B, Macher MA, Lavocat MP, Krier MJ, Baudouin V, Azema C, Bader-Meunier B, Deschenes G (2006) Prognosis of lupus membranous nephropathy in children. Pediatr Nephrol 21:1113–1116

    Article  PubMed  Google Scholar 

  • National High BP Education Program Working Group on High BP in Children and Adolescents, T (2004) The fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. Pediatrics 114:555–576

    Article  Google Scholar 

  • Nee R, Martinez-Osorio J, Yuan CM, Little DJ, Watson MA, Agodoa L, Abbott KC (2015) Survival disparity of African American versus non–African American patients with esrd due to SLE. Am J Kidney Dis 66:630–637

    Article  PubMed  Google Scholar 

  • Nhlbi T (2011) Expert panel on integrated guidelines for cardiovascular health and risk reduction in children and adolescents: summary report. Pediatrics 128:S213–S256

    Article  Google Scholar 

  • Niederer HA, Clatworthy MR, Willcocks LC, Smith KG (2010) FcgammaRIIB, FcgammaRIIIB, and systemic lupus erythematosus. Ann N Y Acad Sci 1183:69–88

    Article  CAS  PubMed  Google Scholar 

  • Nielsen CT, Ostergaard O, Rekvig OP, Sturfelt G, Jacobsen S, Heegaard NH (2015) Galectin-3 binding protein links circulating microparticles with electron dense glomerular deposits in lupus nephritis. Lupus 24:1150–1160

    Article  CAS  PubMed  Google Scholar 

  • Niewold TB, Swedler WI (2005) Systemic lupus erythematosus arising during interferon-alpha therapy for cryoglobulinemic vasculitis associated with hepatitis C. Clin Rheumatol 24:178–181

    Article  PubMed  Google Scholar 

  • Norata GD, Pirillo A, Ammirati E, Catapano AL (2012) Emerging role of high density lipoproteins as a player in the immune system. Atherosclerosis 220:11–21

    Article  CAS  PubMed  Google Scholar 

  • Nossent HC, Swaak TJ, Berden JH (1990) Systemic lupus erythematosus: analysis of disease activity in 55 patients with end-stage renal failure treated with hemodialysis or continuous ambulatory peritoneal dialysis. Dutch Working Party on SLE. Am J Med 89:169–174

    Article  CAS  PubMed  Google Scholar 

  • O’Neill SG, Giles I, Lambrianides A, Manson J, D’Cruz D, Schrieber L, March LM, Latchman DS, Isenberg DA, Rahman A (2010) Antibodies to apolipoprotein A-I, high-density lipoprotein, and C-reactive protein are associated with disease activity in patients with systemic lupus erythematosus. Arthritis Rheum 62:845–854

    Article  PubMed  CAS  Google Scholar 

  • Ophascharoensuk V, Fero ML, Hughes J, Roberts JM, Shankland SJ (1998) The cyclin-dependent kinase inhibitor P27kip1 safeguards against inflammatory injury. Nat Med 4:575–580

    Article  CAS  PubMed  Google Scholar 

  • Pereira T, Abitbol CL, Seeherunvong W, Katsoufis C, Chandar J, Freundlich M, Zilleruelo G (2011) Three decades of progress in treating childhood-onset lupus nephritis. Clin J Am Soc Nephrol 6(9):2192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pereira M, Muscal E, Eldin K, Hicks MJ, Sagcal-Gironella ACP, Deguzman M, Wenderfer SE (2017) Clinical presentation and outcomes of childhood-onset membranous lupus nephritis. Pediatr Nephrol. https://doi.org/10.1007/s00467-017-3743-z

  • Petri MA, Kiani AN, Post W, Christopher-Stine L, Magder LS (2011) Lupus atherosclerosis prevention study (LAPS). Ann Rheum Dis 70(5):760

    Article  CAS  PubMed  Google Scholar 

  • Plazak W, Gryga K, Dziedzic H, Tomkiewicz-Pajak L, Konieczynska M, Podolec P, Musial J (2011) Influence of atorvastatin on coronary calcifications and myocardial perfusion defects in systemic lupus erythematosus patients: a prospective, randomized, double-masked, placebo-controlled study. Arthritis Res Ther 13:R117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 61:830–839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quinlan C, Kari J, Pilkington C, Deanfield J, Shroff R, Marks S, Tullus K (2015) The vascular phenotype of children with systemic lupus erythematosus. Pediatr Nephrol 30:1307–1316

    Article  PubMed  Google Scholar 

  • Radeke HH, Janssen-Graalfs I, Sowa EN, Chouchakova N, Skokowa J, Loscher F, Schmidt RE, Heeringa P, Gessner JE (2002) Opposite regulation of type I and I receptors for immunoglobulin G in mouse glomerular mesangial cells and in the induction of anti-glomerular basement membrane (GBM) nephritis. J Biol Chem 277:27535–27544

    Article  CAS  PubMed  Google Scholar 

  • Rianthavorn P, Buddhasri A (2015) Long-term renal outcomes of childhood-onset global and segmental diffuse proliferative lupus nephritis. Pediatr Nephrol 30:1969–1976

    Article  PubMed  Google Scholar 

  • Robinson AB, Tangpricha V, Yow E, Gurion R, Mccomsey GA, Schanberg LE (2014) Vitamin D deficiency is common and associated with increased C-reactive protein in children and young adults with lupus: an Atherosclerosis Prevention in Pediatric Lupus Erythematosus substudy. Lupus Sci Med 1:E000011

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodd C, Lang B, Ramsay T, Alos N, Huber AM, Cabral DA, Scuccimarri R, Miettunen PM, Roth J, Atkinson SA, Couch R, Cummings EA, Dent PB, Ellsworth J, Hay J, Houghton K, Jurencak R, Larche M, Leblanc C, Oen K, Saint-Cyr C, Stein R, Stephure D, Taback S, Lentle B, Matzinger M, Shenouda N, Moher D, Rauch F, Siminoski K, Ward LM (2012) Incident vertebral fractures among children with rheumatic disorders 12 months after glucocorticoid initiation: a national observational study. Arthritis Care Res 64:122–131

    Article  Google Scholar 

  • Ross AC, Taylor CL, Yaktine AL, Del Valle HB (eds) (2011) Dietary reference intakes for calcium and vitamin D. National Academies Press, Washington, DC

    Google Scholar 

  • Rubtsova K, Marrack P, Rubtsov AV (2015) Sexual dimorphism in autoimmunity. J Clin Invest 125:2187–2193

    Article  PubMed  PubMed Central  Google Scholar 

  • Ruggiero B, Vivarelli M, Gianviti A, Pecoraro C, Peruzzi L, Benetti E, Ventura G, Pennesi M, Murer L, Coppo R, Emma F (2016) Outcome of childhood-onset full-house nephropathy. Nephrol Dial Transplant 32:1194–1204, Pii: Gfw230

    Google Scholar 

  • Sahu R, Bethunaickan R, Singh S, Davidson A (2014) Structure and function of renal macrophages and dendritic cells from lupus-prone mice. Arthritis Rheumatol 66:1596–1607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salloum R, Franek BS, Kariuki SN, Rhee L, Mikolaitis RA, Jolly M, Utset TO, Niewold TB (2010) Genetic variation at the Irf7/Phrf1 locus is associated with autoantibody profile and serum interferon-alpha activity in lupus patients. Arthritis Rheum 62:553–561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samuelson EM, Laird RM, Papillion AM, Tatum AH, Princiotta MF, Hayes SM (2014) Reduced B lymphoid kinase (Blk) expression enhances proinflammatory cytokine production and induces nephrosis in C57bl/6-Lpr/Lpr mice. PLoS One 9:E92054

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sanchez E, Comeau ME, Freedman BI, Kelly JA, Kaufman KM, Langefeld CD, Brown EE, Alarcon GS, Kimberly RP, Edberg JC, Ramsey-Goldman R, Petri M, Reveille JD, Vila LM, Merrill JT, Tsao BP, Kamen DL, Gilkeson GS, James JA, Vyse TJ, Gaffney PM, Jacob CO, Niewold TB, Richardson BC, Harley JB, Alarcon-Riquelme ME, Sawalha AH (2011) Identification of novel genetic susceptibility loci in African American lupus patients in a candidate gene association study. Arthritis Rheum 63:3493–3501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santiago A, Satriano J, Decandido S, Holthofer H, Schreiber R, Unkeless J, Schlondorff D (1989) A specific fc gamma receptor on cultured rat mesangial cells. J Immunol 143:2575–2582

    CAS  PubMed  Google Scholar 

  • Santos MJ, Vinagre F, Silva JJ, Gil V, Fonseca JE (2010) Cardiovascular risk profile in systemic lupus erythematosus and rheumatoid arthritis: a comparative study of female patients. Acta Reumatol Port 35:325–332

    PubMed  Google Scholar 

  • Sawai T, Uzuki M, Satoh N (1995) Kidney disease in systemic lupus erythematosus (SLE) of children – morphometric analysis of kidneys from autopsy cases. Tohoku J Exp Med 177:139–151

    Article  CAS  PubMed  Google Scholar 

  • Schanberg LE, Sandborg C, Barnhart HX, Ardoin SP, Yow E, Evans GW, Mieszkalski KL, Ilowite NT, Eberhard A, Levy DM, Kimura Y, Von Scheven E, Silverman E, Bowyer SL, Punaro L, Singer NG, Sherry DD, Mccurdy D, Klein-Gitelman M, Wallace C, Silver R, Wagner-Weiner L, Higgins GC, Brunner HI, Jung L, Soep JB, Reed A (2009) Premature atherosclerosis in pediatric systemic lupus erythematosus: risk factors for increased carotid intima-media thickness in the atherosclerosis prevention in pediatric lupus erythematosus cohort. Arthritis Rheum 60:1496–1507

    Article  PubMed  PubMed Central  Google Scholar 

  • Schanberg LE, Sandborg C, Barnhart HX, Ardoin SP, Yow E, Evans GW, Mieszkalski KL, Ilowite NT, Eberhard A, Imundo LF, Kimura Y, Von Scheven E, Silverman E, Bowyer SL, Punaro L, Singer NG, Sherry DD, Mccurdy D, Klein-Gitelman M, Wallace C, Silver R, Wagner-Weiner L, Higgins GC, Brunner HI, Jung L, Soep JB, Reed AM, Provenzale J, Thompson SD (2012) Use of atorvastatin in systemic lupus erythematosus in children and adolescents. Arthritis Rheum 64:285–296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwartz MM, Roberts JL, Lewis EJ (1983) Necrotizing glomerulitis of systemic lupus erythematosus. Hum Pathol 14:158–167

    Article  CAS  PubMed  Google Scholar 

  • Sekine H, Ruiz P, Gilkeson GS, Tomlinson S (2011) The dual role of complement in the progression of renal disease in NZB/W F(1) mice and alternative pathway inhibition. Mol Immunol 49:317–323

    Article  CAS  PubMed  Google Scholar 

  • Shafi ST, Gupta M (2007) Risk of vascular access thrombosis in patients with systemic lupus erythematosus on hemodialysis. J Vasc Access 8:103–108

    CAS  PubMed  Google Scholar 

  • Shah K, Lee WW, Lee SH, Kim SH, Kang SW, Craft J, Kang I (2010) Dysregulated balance of Th17 and Th1 cells in systemic lupus erythematosus. Arthritis Res Ther 12:R53

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sharman A, Furness P, Feehally J (2004) Distinguishing C1q nephropathy from lupus nephritis. Nephrol Dial Transplant 19(6):1420

    Article  CAS  PubMed  Google Scholar 

  • Shi H, Yan T, Li D, Jia J, Shang W, Wei L, Zheng Z (2017) Detection of renal hypoxia in lupus nephritis using blood oxygen level-dependent MR imaging: a multiple correspondence analysis. Kidney Blood Press Res 42:123–135

    Article  PubMed  Google Scholar 

  • Shinjo SK, Bonfa E, Wojdyla D, Borba EF, Ramirez LA, Scherbarth HR, Brenol JC, Chacon-Diaz R, Neira OJ, Berbotto GA, De La Torre IG, Acevedo-Vazquez EM, Massardo L, Barile-Fabris LA, Caeiro F, Silveira LH, Sato EI, Buliubasich S, Alarcon GS, Pons-Estel BA (2010) Antimalarial treatment may have a time-dependent effect on lupus survival: data from a multinational latin american inception cohort. Arthritis Rheum 62:855–862

    Article  CAS  PubMed  Google Scholar 

  • Silva CA, Avcin T, Brunner HI (2012) Taxonomy for systemic lupus erythematosus with onset before adulthood. Arthritis Care Res 64:1787–1793

    Article  Google Scholar 

  • Silverman ED, Lang B (1997) An overview of the treatment of childhood SLE. Scand J Rheumatol 26:241–246

    Article  CAS  PubMed  Google Scholar 

  • Simpson N, Gatenby PA, Wilson A, Malik S, Fulcher DA, Tangye SG, Manku H, Vyse TJ, Roncador G, Huttley GA, Goodnow CC, Vinuesa CG, Cook MC (2010) Expansion of circulating t cells resembling follicular helper T cells is a fixed phenotype that identifies a subset of severe systemic lupus erythematosus. Arthritis Rheum 62:234–244

    Article  CAS  PubMed  Google Scholar 

  • Singh S, Abujam B, Gupta A, Suri D, Rawat A, Saikia B, Minz RW, Joshi K, Nada R (2015) Childhood lupus nephritis in a developing country-24 years’ single-center experience from North India. Lupus 24:641–647

    Article  CAS  PubMed  Google Scholar 

  • Siso A, Ramos-Casals M, Bove A, Brito-Zeron P, Soria N, Munoz S, Testi A, Plaza J, Sentis J, Coca A (2008) Previous antimalarial therapy in patients diagnosed with lupus nephritis: influence on outcomes and survival. Lupus 17:281–288

    Article  CAS  PubMed  Google Scholar 

  • Siu YP, Leung KT, Tong MK, Kwan TH, Mok CC (2005) Clinical outcomes of systemic lupus erythematosus patients undergoing continuous ambulatory peritoneal dialysis. Nephrol Dial Transplant 20:2797–2802

    Article  PubMed  Google Scholar 

  • Smet AD, Kuypers D, Evenepoel P, Maes B, Messiaen T, Van Damme B, Vanrenterghem Y (2001) Full house’ positive immunohistochemical membranoproliferative glomerulonephritis in a patient with portosystemic shunt. Nephrol Dial Transplant 16:2258–2262

    Article  CAS  PubMed  Google Scholar 

  • So HC, Gui AH, Cherny SS, Sham PC (2011) Evaluating the heritability explained by known susceptibility variants: a survey of ten complex diseases. Genet Epidemiol 35:310–317

    Article  PubMed  Google Scholar 

  • Somers EC, Marder W, Christman GM, Ognenovski V, Mccune WJ (2005) Use of a gonadotropin-releasing hormone analog for protection against premature ovarian failure during cyclophosphamide therapy in women with severe lupus. Arthritis Rheum 52:2761–2767

    Article  CAS  PubMed  Google Scholar 

  • Sorof JM, Perez MD, Brewer ED, Hawkins EP, Warren RW (1998) Increasing incidence of childhood class V lupus nephritis. J Rheumatol 25:1413–1418

    CAS  PubMed  Google Scholar 

  • Southwest Pediatric Nephrology Study Group, T (1986) Comparison of idiopathic and systemic lupus erythematosus-associated membranous glomerulonephropathy in children. The Southwest Pediatric Nephrology Study Group. Am J Kidney Dis 7:115–124

    Article  Google Scholar 

  • Sozeri B, Deveci M, Dincel N, Mir S (2013) The early cardiovascular changes in pediatric patients with systemic lupus erythematosus. Pediatr Nephrol 28:471–476

    Article  PubMed  Google Scholar 

  • Stagi S, Cavalli L, Bertini F, Martino MD, Cerinic MM, Brandi ML, Falcini F (2014) Vitamin D levels in children, adolescents, and young adults with juvenile-onset systemic lupus erythematosus: a cross-sectional study. Lupus 23:1059–1065

    Article  CAS  PubMed  Google Scholar 

  • Strickland FM, Hewagama A, Wu A, Sawalha AH, Delaney C, Hoeltzel MF, Yung R, Johnson K, Mickelson B, Richardson BC (2013) Diet influences expression of autoimmune associated genes and disease severity by epigenetic mechanisms in a transgenic lupus model. Arthritis Rheum 65:1872–1881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suwanichkul A, Wenderfer SE (2013) Differential expression of functional Fc-receptors and additional immune complex receptors on mouse kidney cells. Mol Immunol 56:369–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swan JT, Riche DM, Riche KD, Majithia V (2011) Systematic review and meta-analysis of immunosuppressant therapy clinical trials in membranous lupus nephritis. J Investig Med 59:246–258

    Article  CAS  PubMed  Google Scholar 

  • Tambralli A, Beukelman T, Cron RQ, Stoll ML (2015) Safety and efficacy of rituximab in childhood-onset systemic lupus erythematosus and other rheumatic diseases. J Rheumatol 42:541–546

    Article  CAS  PubMed  Google Scholar 

  • Tamirou F, D’Cruz D, Sangle S, Remy P, Vasconcelos C, Fiehn C, Ayala Guttierez MDM, Gilboe I-M, Tektonidou M, Blockmans D, Ravelingien I, Le Guern V, Depresseux G, Guillevin L, Cervera R, Houssiau FA, Group, A. T. M. N. T (2015) Long-term follow-up of the MAINTAIN Nephritis Trial, comparing azathioprine and mycophenolate mofetil as maintenance therapy of lupus nephritis. Ann Rheum Dis 75:526–531

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tarr T, Derfalvi B, Gyori N, Szanto A, Siminszky Z, Malik A, Szabo AJ, Szegedi G, Zeher M (2015) Similarities and differences between pediatric and adult patients with systemic lupus erythematosus. Lupus 24:796–803

    Article  CAS  PubMed  Google Scholar 

  • Taylor KE, Remmers EF, Lee AT, Ortmann WA, Plenge RM, Tian C, Chung SA, Nititham J, Hom G, Kao AH, Demirci FY, Kamboh MI, Petri M, Manzi S, Kastner DL, Seldin MF, Gregersen PK, Behrens TW, Criswell LA (2008) Specificity of the STAT4 genetic association for severe disease manifestations of systemic lupus erythematosus. PLoS Genet 4:E1000084

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Taylor KE, Chung SA, Graham RR, Ortmann WA, Lee AT, Langefeld CD, Jacob CO, Kamboh MI, Alarcon-Riquelme ME, Tsao BP, Moser KL, Gaffney PM, Harley JB, Petri M, Manzi S, Gregersen PK, Behrens TW, Criswell LA (2011) Risk alleles for systemic lupus erythematosus in a large case-control collection and associations with clinical subphenotypes. PLoS Genet 7:E1001311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tektonidou MG, Sotsiou F, Nakopoulou L, Vlachoyiannopoulos PG, Moutsopoulos HM (2004) Antiphospholipid syndrome nephropathy in patients with systemic lupus erythematosus and antiphospholipid antibodies: prevalence, clinical associations, and long-term outcome. Arthritis Rheum 50:2569–2579

    Article  PubMed  Google Scholar 

  • Tektonidou MG, Dasgupta A, Ward MM (2016) Risk of end-stage renal disease in patients with lupus nephritis, 1970 to 2015 a systematic review and Bayesian meta-analysis. Arthritis Rheum 68:1432–1441

    Article  Google Scholar 

  • Tesch GH, Maifert S, Schwarting A, Rollins BJ, Kelley VR (1999) Monocyte chemoattractant protein 1-dependent leukocytic infiltrates are responsible for autoimmune disease in MRL-Fas(Lpr) mice. J Exp Med 190:1813–1824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tondel C, Vikse BE, Bostad L, Svarstad E (2012) Safety and complications of percutaneous kidney biopsies in 715 children and 8573 adults in Norway 1988–2010. Clin J Am Soc Nephrol 7:1591–1597

    Article  PubMed  PubMed Central  Google Scholar 

  • Trouw LA, Groeneveld TW, Seelen MA, Duijs JM, 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 114:679–688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsakonas E, Joseph L, Esdaile JM, Choquette D, Senecal JL, Cividino A, Danoff D, Osterland CK, Yeadon C, Smith CD (1998) A long-term study of hydroxychloroquine withdrawal on exacerbations in systemic lupus erythematosus. The Canadian Hydroxychloroquine Study Group. Lupus 7:80–85

    Article  CAS  PubMed  Google Scholar 

  • Tse KC, Li FK, Tang S, Tang CS, Lai KN, Chan TM (2005) Angiotensin inhibition or blockade for the treatment of patients with quiescent lupus nephritis and persistent proteinuria. Lupus 14:947–952

    Article  CAS  PubMed  Google Scholar 

  • Tucci M, Quatraro C, Lombardi L, Pellegrino C, Dammacco F, Silvestris F (2008) Glomerular accumulation of plasmacytoid dendritic cells in active lupus nephritis: role of interleukin-18. Arthritis Rheum 58:251–262

    Article  CAS  PubMed  Google Scholar 

  • Vachvanichsanong P, Dissaneewate P, Mcneil E (2011) Twenty-two years’ experience with childhood-onset SLE in a developing country: are outcomes similar to developed countries? Arch Dis Child 96:44–49

    Article  PubMed  Google Scholar 

  • Vaidya S (2012) Ten-yr renal allograft survival of patients with antiphospholipid antibody syndrome. Clin Transplant 26(6):853

    Article  PubMed  Google Scholar 

  • Vargas-Rojas MI, Crispin JC, Richaud-Patin Y, Alcocer-Varela J (2008) Quantitative and qualitative normal regulatory T cells are not capable of inducing suppression in SLE patients due to T-cell resistance. Lupus 17:289–294

    Article  CAS  PubMed  Google Scholar 

  • Venigalla RK, Tretter T, Krienke S, Max R, Eckstein V, Blank N, Fiehn C, Ho AD, Lorenz HM (2008) Reduced Cd4+,Cd25− T cell sensitivity to the suppressive function of Cd4+,Cd25high,Cd127 −/low regulatory T cells in patients with active systemic lupus erythematosus. Arthritis Rheum 58:2120–2130

    Article  PubMed  Google Scholar 

  • Villanueva E, Yalavarthi S, Berthier CC, Hodgin JB, Khandpur R, Lin AM, Rubin CJ, Zhao W, Olsen SH, Klinker M, Shealy D, Denny MF, Plumas J, Chaperot L, Kretzler M, Bruce AT, Kaplan MJ (2011) Netting neutrophils induce endothelial damage, infiltrate tissues, and expose immunostimulatory molecules in systemic lupus erythematosus. J Immunol 187:538–552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vlahakos DV, Foster MH, Adams S, Katz M, Ucci AA, Barrett KJ, Datta SK, Madaio MP (1992) Anti-DNA antibodies form immune deposits at distinct glomerular and vascular sites. Kidney Int 41:1690–1700

    Article  CAS  PubMed  Google Scholar 

  • Volkmann ER, Grossman JM, Sahakian LJ, Skaggs BJ, Fitzgerald J, Ragavendra N, Charles-Schoeman C, Chen W, Gorn A, Karpouzas G, Weisman M, Wallace DJ, Hahn BH, Mcmahon M (2010) Low physical activity is associated with proinflammatory high-density lipoprotein and increased subclinical atherosclerosis in women with systemic lupus erythematosus. Arthritis Care Res (Hoboken) 62:258–265

    Article  Google Scholar 

  • Vyas S, Hidalgo G, Baqi N, Von Gizyki H, Singh A (2002) Outcome in African-American children of neuropsychiatric lupus and lupus nephritis. Pediatr Nephrol 17:45–49

    Article  PubMed  Google Scholar 

  • Waehre T, Yndestad A, Smith C, Haug T, Tunheim SH, Gullestad L, Froland SS, Semb AG, Aukrust P, Damas JK (2004) Increased expression of interleukin-1 in coronary artery disease with downregulatory effects of HMG-CoA reductase inhibitors. Circulation 109:1966–1972

    Article  CAS  PubMed  Google Scholar 

  • Waters ST, Mcduffie M, Bagavant H, Deshmukh US, Gaskin F, Jiang C, Tung KS, Fu SM (2004) Breaking tolerance to double stranded DNA, nucleosome, and other nuclear antigens is not required for the pathogenesis of lupus glomerulonephritis. J Exp Med 199:255–264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watson L, Beresford MW, Maynes C, Pilkington C, Marks SD, Glackin Y, Tullus K (2015) The indications, efficacy and adverse events of rituximab in a large cohort of patients with juvenile-onset SLE. Lupus 24:10–17

    Article  CAS  PubMed  Google Scholar 

  • 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 15:241–250

    Article  PubMed  Google Scholar 

  • Weidenbusch M, Römmele C, Schröttle A, Anders H-J (2013) Beyond the LUNAR trial. Efficacy of rituximab in refractory lupus nephritis. Nephrol Dial Transplant 28:106–111

    Article  CAS  PubMed  Google Scholar 

  • Wenderfer SE, Soimo K, Wetsel RA, Braun MC (2007) Analysis of C4 and the C4 binding protein in the Mrl/Lpr mouse. Arthritis Res Ther 9:R114

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wenderfer SE, Lane JC, Shatat IF, Von Scheven E, Ruth NM (2015) Practice patterns and approach to kidney biopsy in lupus: a collaboration of the Midwest pediatric nephrology consortium and the childhood arthritis and rheumatology research alliance. Pediatr Rheumatol 13:26

    Article  Google Scholar 

  • Weng CH, Hsu CW, Yu CC, Yen TH, Yang CW, Hung CC (2009) Peritoneal dialysis and hemodialysis in systemic lupus erythematosus patients: comparison of clinical outcomes. Kidney Blood Press Res 32(6):451

    Article  PubMed  Google Scholar 

  • Willems M, Haddad E, Niaudet P, Kone-Paut I, Bensman A, Cochat P, Deschenes G, Fakhouri F, Leblanc T, Llanas B, Loirat C, Pillet P, Ranchin B, Salomon R, Ulinski T, Bader-Meunier B (2006) Rituximab therapy for childhood-onset systemic lupus erythematosus. J Pediatr 148:623–627

    Article  CAS  PubMed  Google Scholar 

  • Winchester R, Wiesendanger M, Zhang HZ, Steshenko V, Peterson K, Geraldino-Pardilla L, Ruiz-Vazquez E, D’Agati V (2012) Immunologic characteristics of intrarenal t cells: trafficking of expanded Cd8+ T cell beta-chain clonotypes in progressive lupus nephritis. Arthritis Rheum 64:1589–1600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wong SN, Chan WK, Hui J, Chim S, Lee TL, Lee KP, Leung LC, Tse NK, Yuen SF (2009) Membranous lupus nephritis in Chinese children – a case series and review of the literature. Pediatr Nephrol 24:1989–1996

    Article  PubMed  Google Scholar 

  • Woo JM, Lin Z, Navab M, Van Dyck C, Trejo-Lopez Y, Woo KM, Li H, Castellani LW, Wang X, Iikuni N, Rullo OJ, Wu H, La Cava A, Fogelman AM, Lusis AJ, Tsao BP (2010) Treatment with apolipoprotein A-1 mimetic peptide reduces lupus-like manifestations in a murine lupus model of accelerated atherosclerosis. Arthritis Res Ther 12:R93

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu JY, Yeh KW, Huang JL (2013) Early predictors of outcomes in pediatric lupus nephritis: focus on proliferative lesions. Semin Arthritis Rheum 43:513–520

    Article  PubMed  Google Scholar 

  • Yang W, Tang H, Zhang Y, Tang X, Zhang J, Sun L, Yang J, Cui Y, Zhang L, Hirankarn N, Cheng H, Pan HF, Gao J, Lee TL, Sheng Y, Lau CS, Li Y, Chan TM, Yin X, Ying D, Lu Q, Leung AM, Zuo X, Chen X, Tong KL, Zhou F, Diao Q, Tse NK, Xie H, Mok CC, Hao F, Wong SN, Shi B, Lee KW, Hui Y, Ho MH, Liang B, Lee PP, Cui H, Guo Q, Chung BH, Pu X, Liu Q, Zhang X, Zhang C, Chong CY, Fang H, Wong RW, Sun Y, Mok MY, Li XP, Avihingsanon Y, Zhai Z, Rianthavorn P, Deekajorndej T, Suphapeetiporn K, Gao F, Shotelersuk V, Kang X, Ying SK, Wong WH, Zhu D, Fung SK, Zeng F, Lai WM, Wong CM, Ng IO, Garcia-Barcelo MM, Cherny SS, Shen N, Tam PK, Sham PC, Ye DQ, Yang S, Lau YL (2013) Meta-analysis followed by replication identifies loci in or near Cdkn1b, Tet3, Cd80, Dram1, and Arid5b as associated with systemic lupus erythematosus in Asians. Am J Hum Genet 92:41–51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan J, Zhao D, Wu L, Xu X, Pang Y, Zhang J, Ma Y, Liu J, Wang J (2015) Fcgr3b copy number loss rather than gain is a risk factor for systemic lupus erythematous and lupus nephritis: a meta-analysis. Int J Rheum Dis 18:392–397

    Article  CAS  PubMed  Google Scholar 

  • Yung S, Cheung KF, Zhang Q, Chan TM (2010) Anti-dsDNA antibodies bind to mesangial annexin II in lupus nephritis. J Am Soc Nephrol 21(11):1912–1927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zamora-Ustaran A, Escarcega-Alarcon RO, Garcia-Carrasco M, Faugier E, Mendieta-Zeron S, Mendoza-Pinto C, Montiel-Jarquin A, Munoz-Guarneros M, Lopez-Colombo A, Cervera R (2012) Antiphospholipid syndrome in Mexican children. Isr Med Assoc J 14:286–289

    PubMed  Google Scholar 

  • Zappitelli M, Duffy C, Bernard C, Scuccimarri R, Watanabe Duffy K, Kagan R, Gupta IR (2004) Clinicopathological study of the WHO classification in childhood lupus nephritis. Pediatr Nephrol 19:503–510

    Article  PubMed  Google Scholar 

  • Zappitelli M, Duffy CM, Bernard C, Gupta IR (2008) Evaluation of activity, chronicity and tubulointerstitial indices for childhood lupus nephritis. Pediatr Nephrol 23:83–91

    Article  PubMed  Google Scholar 

  • Zhang Y, Yang J, Jiang S, Fang C, Xiong L, Cheng H, Xia Y (2012) The lupus-derived anti-double-stranded DNA IgG contributes to myofibroblast-like phenotype in mesangial cells. J Clin Immunol 32:1270–1278

    Article  CAS  PubMed  Google Scholar 

  • Zhou TB, Liu YG, Lin N, Qin YH, Huang K, Shao MB, Peng DD (2012) Relationship between angiotensin-converting enzyme insertion/deletion gene polymorphism and systemic lupus erythematosus/lupus nephritis: a systematic review and metaanalysis. J Rheumatol 39:686–693

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Scott E. Wenderfer .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG

About this entry

Cite this entry

Wenderfer, S.E., Ruth, N.M. (2018). Lupus Nephritis (Including Antiphospholipid Antibody Syndrome), Pediatric. In: Trachtman, H., Hogan, J., Herlitz, L., Lerma, E. (eds) Glomerulonephritis. Springer, Cham. https://doi.org/10.1007/978-3-319-27334-1_15-1

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-27334-1_15-1

  • Received:

  • Accepted:

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-27334-1

  • Online ISBN: 978-3-319-27334-1

  • eBook Packages: Springer Reference MedicineReference Module Medicine

Publish with us

Policies and ethics