European evidence-based recommendations for the diagnosis and treatment of childhood-onset lupus nephritis: The SHARE initiative

Annals of the Rheumatic Diseases

Volumn 76, Issue 12, 2017, Pages 1965-1973

  Groot, Noortje ^a,b   De Graeff, Nienke ^a   Marks, Stephen D ^c   Brogan, Paul ^c   Avcin, Tadej ^d   Bader Meunier, Brigitte ^e   Dolezalova, Pavla ^f   Feldman, Brian M ^g   Kone Paut, Isabelle ^h   Lahdenne, Pekka ⁱ   McCann, Liza ^j   Özen, Seza ^k   Pilkington, Clarissa A ^c   Ravelli, Angelo ^l   Van Royen Kerkhof, Annet ^a   Uziel, Yosef ^m   Vastert, Bas J ^a   Wulffraat, Nico M ^a   Beresford, Michael W ^j,n   Kamphuis, Sylvia ^b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b SOPHIA CHILDREN S HOSPITAL   (Netherlands)

^c GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^d UNIVERSITY CHILDREN S HOSPITAL   (Slovenia)

^e HÔPITAL NECKER ENFANTS MALADES   (France)

^f CHARLES UNIVERSITY   (Czech Republic)

^g HOSPITAL FOR SICK CHILDREN   (Canada)

^h BICÊTRE HOSPITAL   (France)

ⁱ UNIVERSITY OF HELSINKI   (Finland)

^j ALDER HEY CHILDREN'S NHS FOUNDATION TRUST   (United Kingdom)

^k HACETTEPE UNIVERSITY   (Turkey)

^l UNIVERSITY OF GENOA   (Italy)

^m TEL AVIV UNIVERSITY   (Israel)

ⁿ UNIVERSITY OF LIVERPOOL   (United Kingdom)

more..

Author keywords

corticosteroids; disease activity; lupus nephritis; systemic lupus erythematosus; treatment

Indexed keywords

AZATHIOPRINE; CORTICOSTEROID; CYCLOPHOSPHAMIDE; DISEASE MODIFYING ANTIRHEUMATIC DRUG; MYCOPHENOLATE MOFETIL; PREDNISONE; ANTIRHEUMATIC AGENT; IMMUNOSUPPRESSIVE AGENT; MYCOPHENOLIC ACID;

ARTICLE; CHILD HEALTH CARE; CHILDHOOD ONSET LUPUS NEPHRITIS; DIAGNOSTIC PROCEDURE; DISEASE CLASSIFICATION; EVIDENCE BASED PRACTICE; HEALTH CARE QUALITY; HUMAN; LOW DRUG DOSE; LUPUS ERYTHEMATOSUS NEPHRITIS; MAINTENANCE THERAPY; PRACTICE GUIDELINE; PROTEINURIA; SYSTEMATIC REVIEW; TIME TO TREATMENT; TREATMENT DURATION; CHILD; DISEASE MANAGEMENT; EUROPE; EVIDENCE BASED MEDICINE; ONSET AGE; PROCEDURES; REMISSION; STANDARDS; TREATMENT OUTCOME;

ADRENAL CORTEX HORMONES; AGE OF ONSET; ANTIRHEUMATIC AGENTS; AZATHIOPRINE; CHILD; CYCLOPHOSPHAMIDE; DISEASE MANAGEMENT; EUROPE; EVIDENCE-BASED MEDICINE; HUMANS; IMMUNOSUPPRESSIVE AGENTS; LUPUS NEPHRITIS; MYCOPHENOLIC ACID; PRACTICE GUIDELINES AS TOPIC; REMISSION INDUCTION; TREATMENT OUTCOME;

EID: 85037715187     PISSN: 00034967     EISSN: 14682060     Source Type: Journal    
DOI: 10.1136/annrheumdis-2017-211898     Document Type: Article

References (90)

1. Wulffraat NM, Vastert B. Time to share. Pediatr Rheumatol Online J 2013;11:5.
2. Hiraki LT, Feldman CH, Liu J, et al. Prevalence, incidence, and demographics of systemic lupus erythematosus and lupus nephritis from 2000 to 2004 among children in the US medicaid beneficiary population. Arthritis & Rheumatism 2012;64:2669-76.
3. Kamphuis S, Silverman ED. Prevalence and burden of pediatric-onset systemic lupus erythematosus. Nat Rev Rheumatol 2010;6:538-46.
4. Pineles D, Valente A, Warren B, et al. Worldwide incidence and prevalence of pediatric onset systemic lupus erythematosus. Lupus 2011;20:1187-92.
5. Bader-Meunier B, Armengaud JB, Haddad E, et al. Initial presentation of childhoodonset systemic lupus erythematosus: A French multicenter study. J Pediatr 2005;146:648-53.
6. Font J, Cervera R, Espinosa G, et al. Systemic lupus erythematosus (SLE) in childhood: Analysis of clinical and immunological findings in 34 patients and comparison with SLE characteristics in adults. Ann Rheum Dis 1998;57:456-9.
7. Ramirez Gomez LA, Uribe Uribe O, Osio Uribe O, et al. Childhood systemic lupus erythematosus in Latin America. The GLADEL experience in 230 children. Lupus 2008;17:596-604.
8. Watson L, Leone V, Pilkington C, et al. Disease activity, severity, and damage in the UK juvenile-onset systemic lupus erythematosus cohort. Arthritis & Rheumatism 2012;64:2356-65.
9. Bertsias GK, Tektonidou M, Amoura Z, et al. Joint European league against rheumatism and European renal Association-European dialysis and transplant association (EULAR/ERA-EDTA) recommendations for the management of adult and paediatric lupus nephritis. Ann Rheum Dis 2012;71:1771-82.
10. Mina R, von Scheven E, Ardoin SP, et al. Consensus treatment plans for induction therapy of newly diagnosed proliferative lupus nephritis in juvenile systemic lupus erythematosus. Arthritis Care Res 2012;64:375-83.
11. Enders FB, Bader-Meunier B, Baildam E, et al. Consensus-based recommendations for the management of juvenile dermatomyositis. Ann Rheum Dis 2017;76:329-40.
12. Giancane G, Ter Haar NM, Wulffraat N, et al. Evidence-based recommendations for genetic diagnosis of familial Mediterranean fever. Ann Rheum Dis 2015;74:635-41.
13. ter Haar NM, Oswald M, Jeyaratnam J, et al. Recommendations for the management of autoinflammatory diseases. Ann Rheum Dis 2015;74:1636-44.
14. Groot N, de Graeff N, Avcin T, et al. European evidence-based recommendations for diagnosis and treatment of paediatric antiphospholipid syndrome: The SHARE initiative. Ann Rheum Dis 2017;76:1637-41.
15. Groot N, de Graeff N, Avcin T, et al. European evidence-based recommendations for diagnosis and treatment of childhood-onset systemic lupus erythematosus: The SHARE initiative. Ann Rheum Dis 2017;76:1788-96.
16. Dougados M, Betteridge N, Burmester GR, et al. EULAR standardised operating procedures for the elaboration, evaluation, dissemination, and implementation of recommendations endorsed by the EULAR standing committees. Ann Rheum Dis 2004;63:1172-6.
17. Leclercq E, Leeflang MMG, van Dalen EC, et al. Validation of search filters for identifying pediatric studies in PubMed. J Pediatr 2013;162:629-34.
18. Groot N, de Graeff N, Avcin T, et al. European evidence-based recommendations for diagnosis and treatment of childhood-onset systemic lupus erythematosus: The SHARE initiative. Ann Rheum Dis 2017;76:1788-96.
19. Zhang W, Doherty M, Pascual E, et al. EULAR evidence based recommendations for gout. Part I: Diagnosis. Report of a task force of the standing committee for international clinical studies including therapeutics (ESCISIT). Ann Rheum Dis 2006;65:1301-11.
20. Zhang W, Doherty M, Bardin T, et al. EULAR evidence based recommendations for gout. Part II: Management. Report of a task force of the EULAR Standing Committee for International Clinical Studies Including Therapeutics (ESCISIT). Ann Rheum Dis 2006;65:1312-24.
21. vdVA DAL. A group process model for problem identification and program planning. J Appl Behav Sci 1971;7:466-92.
22. Chandar J, Gomez-Marin O, del Pozo R, et al. Role of routine urinalysis in asymptomatic pediatric patients. Clin Pediatr 2005;44:43-8.
23. Sebestyen JF, Alon US. The teenager with asymptomatic proteinuria: Think orthostatic first. Clin Pediatr 2011;50:179-82.
24. Weening JJ, D'agati VD, Schwartz MM, et al. The classification of glomerulonephritis in systemic lupus erythematosus revisited. Kidney Int 2004;65:521-30.
25. Marks SD, Sebire NJ, Pilkington C, et al. Clinicopathological correlations of paediatric lupus nephritis. Pediatric Nephrology 2007;22:77-83.
26. Yokoyama H, Wada T, Hara A, et al. The outcome and a new ISN/RPS 2003 classification of lupus nephritis in Japanese. Kidney Int 2004;66:2382-8.
27. Grootscholten C, Bajema IM, Florquin S, et al. Interobserver agreement of scoring of histopathological characteristics and classification of lupus nephritis. Nephrol Dial Transplant 2008;23:223-30.
28. Lee SG, Cho YM, So MW, et al. ISN/RPS 2003 class II mesangial proliferative lupus nephritis: A comparison between cases that progressed to class III or IV and cases that did not. Rheumatol Int 2012;32:2459-64.
29. Ataei N, Haydarpour M, Madani A, et al. Outcome of lupus nephritis in Iranian children: prognostic significance of certain features. Pediatr Nephrol 2008;23:749-55.
30. Emre S, Bilge I, Sirin A, et al. Lupus nephritis in children: prognostic significance of clinicopathological findings. Nephron 2001;87:118-26.
31. Hobbs DJ, Barletta G-M, Rajpal JS, et al. Severe paediatric systemic lupus erythematosus nephritis-a single-centre experience. Nephrol Dial Transplant 2010;25:457-63.
32. Austin HA, Illei GG, Braun MJ, et al. Randomized, controlled trial of prednisone, cyclophosphamide, and cyclosporine in lupus membranous nephropathy. J Am Soc Nephrol 2009;20:901-11.
33. Radhakrishnan J, Moutzouris D-A, Ginzler EM, et al. Mycophenolate mofetil and intravenous cyclophosphamide are similar as induction therapy for class V lupus nephritis. Kidney Int 2010;77:152-60.
34. Mercadal L, et al. Factors affecting outcome and prognosis in membranous lupus nephropathy. Nephrology Dialysis Transplantation 2002;17:1771-8.
35. Mok CC, Ying KY, Lau CS, et al. Treatment of pure membranous lupus nephropathy with prednisone and azathioprine: An open-label trial. American Journal of Kidney Diseases 2004;43:269-76.
36. Sloan RP, Schwartz MM, Korbet SM, et al. Long-term outcome in systemic lupus erythematosus membranous glomerulonephritis. Lupus Nephritis Collaborative Study Group. J Am Soc Nephrol 1996;7:299-305.
37. Kanda H, Kubo K, Tateishi S, et al. Antiproteinuric effect of ARB in lupus nephritis patients with persistent proteinuria despite immunosuppressive therapy. Lupus 2005;14:288-92.
38. Tse KC, Li FK, Tang S, et al. Angiotensin inhibition or blockade for the treatment of patients with quiescent lupus nephritis and persistent proteinuria. Lupus 2005;14:947-52.
39. Mok CC, Cheung TT, Lo WH. Minimal mesangial lupus nephritis: A systematic review. Scand J Rheumatol 2010;39:181-9.
40. Marks SD, Shah V, Pilkington C, et al. Renal tubular dysfunction in children with systemic lupus erythematosus. Pediatric Nephrology 2005;20:141-8.
41. Han TS, Schwartz MM, Lewis EJ. Association of glomerular podocytopathy and nephrotic proteinuria in mesangial lupus nephritis. Lupus 2006;15:71-5.
42. Hertig A, Droz D, Lesavre P, et al. SLE and idiopathic nephrotic syndrome: Coincidence or not American Journal of Kidney Diseases 2002;40:1179-84.
43. Taheri S, Beiraghdar F. Lupus nephritis in Iranian children: A review of 60 patients. Ren Fail 2011;33:499-505.
44. Tanaka H, Oki E, Tsuruga K, et al. Management of young patients with lupus nephritis using tacrolimus administered as a single daily dose. Clin Nephrol 2009;72:430-6.
45. Trachana M, Koutsonikoli A, Farmaki E, et al. Safety and efficacy of Rituximab in refractory pediatric systemic lupus erythematosus nephritis: A single-center experience of Northern Greece. Rheumatol Int 2013;33:809-13.
46. Ruggiero B, Vivarelli M, Gianviti A, et al. Lupus nephritis in children and adolescents: results of the Italian Collaborative Study. Nephrol Dial Transplant 2013;28:1487-96.
47. Bogdanovi R, Nikoli V, Paši S, et al. Lupus nephritis in childhood: A review of 53 patients followed at a single center. Pediatr Nephrol 2004;19:36-44.
48. Khoo JJ, Pee S. Thevarajah B, Yap YC, Chin CK. Lupus nephritis in children in Malaysia. J Paediatr Child Health 2005;41(1-2):31-5.
49. Lee BS, Cho HY, Kim EJ, et al. Clinical outcomes of childhood lupus nephritis: A single center's experience. Pediatr Nephrol 2006;22:222-31.
50. Houssiau FA, Vasconcelos C, D'Cruz D, et al. Immunosuppressive therapy in lupus nephritis: The Euro-Lupus Nephritis Trial, a randomized trial of low-dose versus high-dose intravenous cyclophosphamide. Arthritis & Rheumatism 2002;46:2121-31.
51. Ginzler EM, Dooley MA, Aranow C, et al. Mycophenolate mofetil or intravenous cyclophosphamide for lupus nephritis. N Engl J Med Overseas Ed 2005;353:2219-28.
52. Palmer SC, Tunnicliffe DJ, Singh-Grewal D, et al. Induction and maintenance immunosuppression treatment of proliferative lupus nephritis: A network metaanalysis of randomized trials. Am J Kidney Dis 2017.
53. Askenazi D, Myones B, Kamdar A, et al. Outcomes of children with proliferative lupus nephritis: The role of protocol renal biopsy. Pediatr Nephrol 2007;22:981-6.
54. Baqi N, Moazami S, Singh A, et al. Lupus nephritis in children: A longitudinal study of prognostic factors and therapy. J Am Soc Nephrol 1996;7:924-9.
55. Barbano G, Gusmano R, Damasio B, et al. Childhood-onset lupus nephritis: A single-center experience of pulse intravenous cyclophosphamide therapy. J Nephrol 2002;15:123-9.
56. Baskin E, Ozen S, Cakar N, et al. The use of low-dose cyclophosphamide followed by AZA/MMF treatment in childhood lupus nephritis. Pediatr Nephrol 2010;25:111-7.
57. Benseler SM, Bargman JM, Feldman BM, et al. Acute renal failure in paediatric systemic lupus erythematosus: Treatment and outcome. Rheumatology 2009;48:176-82.
58. Chiu S-J, Ou L-S, Tsai T-L, et al. Sequential evaluation of clinical and laboratory changes amongst children suffering from lupus nephritis during intermittent intravenous cyclophosphamide therapy. Clin Rheumatol 2006;25:515-9.
59. Hagelberg S, Lee Y, Bargman J, et al. Longterm followup of childhood lupus nephritis. J Rheumatol 2002;29:2635-42.
60. Lau KK, Ault BH, Jones DP, et al. Induction therapy for pediatric focal proliferative lupus nephritis: cyclophosphamide versus mycophenolate mofetil. Journal of Pediatric Health Care 2008;22:282-8.
61. Lehman TJA, Sherry DD, Wagner-Weiner L, et al. Intermittent intravenous cyclophosphamide therapy for lupus nephritis. J Pediatr 1989;114:1055-60.
62. Buratti S, Szer IS, Spencer CH, et al. Mycophenolate mofetil treatment of severe renal disease in pediatric onset systemic lupus erythematosus. J Rheumatol 2001;28:2103-8.
63. Aragon E, Chan YH, Ng KH, Kh N, et al. Good outcomes with mycophenolatecyclosporine-based induction protocol in children with severe proliferative lupus nephritis. Lupus 2010;19:965-73.
64. Tamirou F, D'Cruz D, Sangle S, et al. Long-term follow-up of the MAINTAIN Nephritis Trial, comparing azathioprine and mycophenolate mofetil as maintenance therapy of lupus nephritis. Ann Rheum Dis 2016;75:526-31.
65. Dooley MA, Jayne D, Ginzler EM, et al. Mycophenolate versus Azathioprine as Maintenance Therapy for Lupus Nephritis. N Engl J Med Overseas Ed 2011;365:1886-95.
66. Appel GB, Contreras G, Dooley MA, et al. Mycophenolate versus azathioprine as maintenance therapy for lupus nephritis. J Am Soc Nephrol 2009;20:1103-12.
67. Vachvanichsanong P, Dissaneewate P, McNeil E. Intravenous cyclophosphamide combined with steroids in pediatric onset severe lupus nephritis. Int Urol Nephrol 2013;45:1301-8.
68. Vachvanichsanong P, Dissaneewate P, Winn T. Intravenous cyclophosphamide for lupus nephritis in Thai children. Scand J Rheumatol 2004;33:339-42.
69. Tamirou F, Husson SN, Gruson D, et al. Brief Report: The Euro-Lupus Low-Dose Intravenous Cyclophosphamide Regimen Does Not Impact the Ovarian Reserve, as Measured by Serum Levels of Anti-Mullerian Hormone. Arthritis Rheumatol 2017;69:1267-71.
70. Henderson LK, Masson P, Craig JC, et al. Induction and maintenance treatment of proliferative lupus nephritis: A meta-analysis of randomized controlled trials. Am J Kidney Dis 2013;61:74-87.
71. Houssiau FA, D'Cruz D, Sangle S, et al. Azathioprine versus mycophenolate mofetil for long-term immunosuppression in lupus nephritis: results from the MAINTAIN Nephritis Trial. Ann Rheum Dis 2010;69:2083-9.
72. Demircin G, Oner A, Erdoan Ozlem, et al. Long-term efficacy and safety of quadruple therapy in childhood diffuse proliferative lupus nephritis. Ren Fail 2008;30:603-9.
73. Pereira T, Abitbol CL, Seeherunvong W, et al. Three decades of progress in treating childhood-onset lupus nephritis. Clin J Am Soc Nephrol 2011;6:2192-9.
74. Brunner HI, Bishnoi A, Barron AC, et al. Disease outcomes and ovarian function of childhood-onset systemic lupus erythematosus. Lupus 2006;15:198-206.
75. Hahn BH, McMahon MA, Wilkinson A, et al. American College of Rheumatology guidelines for screening, treatment, and management of lupus nephritis. Arthritis Care Res 2012;64:797-808.
76. Renal Disease Subcommittee of the American College of Rheumatology Ad Hoc Committee on Systemic Lupus Erythematosus Response Criteria. The American College of Rheumatology response criteria for proliferative and membranous renal disease in systemic lupus erythematosus clinical trials. Arthritis Rheum 2006;54:421-32.
77. Hugle B, Silverman ED, Tyrrell PN, et al. Presentation and outcome of paediatric membranous non-proliferative lupus nephritis. Pediatr Nephrol 2015;30:113-21.
78. Koneru S, Kocharla L, Higgins GC, et al. Adherence to medications in systemic lupus erythematosus. J Clin Rheumatol 2008;14:195-201.
79. M. R. Adherence to Pediatric Medical Regimens. Handbook of Child Psychology and Developmental Science. 7 edn. New York: John Wiley & Sons Inc, 2010:596.
80. Rojas-Serrano J, Cardiel MH. Lupus patients in an emergency unit. Causes of consultation, hospitalization and outcome. A cohort study. Lupus 2000;9:601-6.
81. Uribe AG, Alarcon GS, Sanchez ML, et al. Systemic lupus erythematosus in three ethnic groups. XVIII. Factors predictive of poor compliance with study visits. Arthritis Care Res 2004;51:258-63.
82. Elmougy A, Sarhan A, Hammad A, et al. Lupus nephritis in Egyptian children: A 16-year experience. J Nephrol 2015;28:557-62.
83. Srivastava P, Abujam B, Misra R, et al. Outcome of lupus nephritis in childhood onset SLE in North and Central India: single-centre experience over 25 years. Lupus 2016;25:547-57.
84. Merrill JT, Neuwelt CM, Wallace DJ, et al. Efficacy and safety of rituximab in moderately-to-severely active systemic lupus erythematosus: The randomized, doubleblind, phase ii/iii systemic lupus erythematosus evaluation of rituximab trial. Arthritis & Rheumatism 2010;62:222-33.
85. Rovin BH, Furie R, Latinis K, et al. Efficacy and safety of rituximab in patients with active proliferative lupus nephritis: The lupus nephritis assessment with rituximab study. Arthritis & Rheumatism 2012;64:1215-26.
86. Weidenbusch M, Rommele C, Schrottle A, et al. Beyond the LUNAR trial. Efficacy of rituximab in refractory lupus nephritis. Nephrol Dial Transplant 2013;28:106-11.
87. Bang S-Y, Lee CK, Kang YM, et al. Multicenter retrospective analysis of the effectiveness and safety of rituximab in korean patients with refractory systemic lupus erythematosus. Autoimmune Dis 2012;2012:1-6.
88. Watson L, Beresford MW, Maynes C, et al. The indications, efficacy and adverse events of rituximab in a large cohort of patients with juvenile-onset SLE. Lupus 2015;24:10-17.
89. Nakamura T, Nozu K, Iijima K, et al. Association of cumulative cyclosporine dose with its irreversible nephrotoxicity in Japanese patients with pediatric-onset autoimmune diseases. Biol Pharm Bull 2007;30:2371-5.
90. Foster HE, Minden K, Clemente D, et al. EULAR/PReS standards and recommendations for the transitional care of young people with juvenile-onset rheumatic diseases. Ann Rheum Dis 2017;76:639-46.