Skip to main content

Advertisement

Log in

Management and outcomes in children with lupus nephritis in the developing countries

  • Systematic Review/Meta-analysis
  • Published:
Pediatric Nephrology Aims and scope Submit manuscript

Abstract

Background

Lupus nephritis (LN) has variable prevalence, severity, and outcomes across the world.

Objectives

This review compares the outcomes of childhood LN in low- and middle-income countries (LMICs) and high-income countries (HICs) and aims to summarize long-term outcomes of pediatric LN from LMICs.

Data sources

A systematic literature search, conducted in PubMed, EMBASE, and Cochrane database in the last 30-years from January 1992, published in the English language, identified 113 studies including 52 from lower (n = 1336) and upper MICs (n = 3014).

Study eligibility criteria

Cohort studies or randomized controlled trials, of patients ≤ 18 years of age (or where such data can be separately extracted), with > 10 patients with clinically or histologically diagnosed LN and outcomes reported beyond 12 months were included.

Participants and interventions

Patients ≤ 18 years of age with clinically or histologically diagnosed LN; effect of an intervention was not measured.

Study appraisal and synthesis methods

Two authors independently extracted data. We separately analyzed studies from developed countries (high income countries; HIC) and developing countries (LMICs). Middle-income countries were further classified as lower and upper MICs. Meta-analyses of data were performed by calculating a pooled estimate utilizing the random-effects model. Test for heterogeneity was applied using I2 statistics. Publication bias was assessed using funnel plots.

Results

Kidney remission was similar across MICs and HICs with 1-year pooled complete remission rates of 59% (95% CI 51–67%); one third of patients had kidney flares. The pooled 5-year survival free of stage 5 chronic kidney disease (CKD5) was lower in MICs, especially in lower MICs compared to HICs (83% vs. 93%; P = 0.002). The pooled 5-year patient survival was significantly lower in MICs than HICs (85% vs. 94%; P < 0.001). In patients with class IV LN, the 5-and 10-year respective risk of CKD5 was 14% and 30% in MICs; corresponding risks in HICs were 8% and 17%. Long-term data from developing countries was limited. Sepsis (48.8%), kidney failure (14%), lupus activity (18.1%), and intracranial hemorrhage/infarct (5.4%) were chief causes of death; mortality due to complications of kidney failure was more common in lower MICs (25.6%) than HICs (6.4%).

Limitations

The review is limited by heterogenous approach to diagnosis and management that has changed over the period spanning the review. World Bank classification based on income might not correlate with the standards of medical care. The overall quality of evidence is low since included studies were chiefly retrospective and single center.

Conclusions and implications of key findings

Challenges in LMICs include limited access to pediatric nephrology care, dialysis, increased risk of infection-induced mortality, lack of frequent monitoring, and non-compliance due to cost of therapy. Attention to these issues might update the existing data and improve patient follow-up and outcomes.

Systematic review registration number

PROSPERO 2022 number: CRD42022359002, available from: https://www.crd.york.ac.uk/prospero/display_record.php?ID=CRD42022359002

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Huang X, Jia N, Xiao F, Sun C, Zhu J, Lai J, Cui X (2022) Differences in the clinical manifestations and mortality of systemic lupus erythematosus onset in children and adults: a systematic review and meta-analysis. Int Arch Allergy Immunol 183:116–126

    Article  CAS  PubMed  Google Scholar 

  2. 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 6:2192–2199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Singh S, Devidayal KL, Joshi K (2002) Mortality patterns in childhood lupus–10 years’ experience in a developing country. Clin Rheumatol 21:462–465

    Article  CAS  PubMed  Google Scholar 

  4. Lewandowski LB, Watt MH, Schanberg LE, Thielman NM, Scott C (2017) Missed opportunities for timely diagnosis of pediatric lupus in South Africa: a qualitative study. Pediatr Rheumatol Online J 15:14

    Article  PubMed  PubMed Central  Google Scholar 

  5. World Bank. Data: country classification, low-income countries. World Bank Country and Lending Groups (2022). http://datahelpdesk.worldbank.org/khnowledgebase/articles/906519 (6 April 2022, date last accessed)

  6. Drevon D, Fursa SR, Malcolm AL (2017) Intercoder reliability and validity of webplotdigitizer in extracting graphed data. Behav Modif 41:323–339

    Article  PubMed  Google Scholar 

  7. Vazzana KM, Daga A, Goilav B, Ogbu EA, Okamura DM, Park C, Sadun RE, Smitherman EA, Stotter BR, Dasgupta A, Knight AM, Hersh AO, Wenderfer SE, Lewandowski LB, Registry Investigators CARRA (2021) Principles of pediatric lupus nephritis in a prospective contemporary multi-center cohort. Lupus 30:1660–1670

    Article  PubMed  Google Scholar 

  8. Smith EMD, Yin P, Jorgensen AL, Beresford MW (2018) Clinical predictors of active LN development in children - evidence from the UK JSLE Cohort Study. Lupus 27:2020–2028

    Article  CAS  PubMed  Google Scholar 

  9. Massias JS, Smith EM, Al-Abadi E, Armon K, Bailey K, Ciurtin C, Davidson J, Gardner-Medwin J, Haslam K, Hawley DP, Leahy A, Leone V, McErlane F, Mewar D, Modgil G, Moots R, Pilkington C, Ramanan AV, Rangaraj S, Riley P, Sridhar A, Wilkinson N, Beresford MW, Hedrich CM (2021) Clinical and laboratory phenotypes in juvenile-onset systemic lupus erythematosus across ethnicities in the UK. Lupus 30:597–607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Maningding E, Dall’Era M, Trupin L, Murphy LB, Yazdany J (2020) Racial and ethnic differences in the prevalence and time to onset of manifestations of systemic lupus erythematosus: the California Lupus Surveillance Project. Arthritis Care Res (Hoboken) 72:622–629

    Article  PubMed  Google Scholar 

  11. Hiraki LT, Benseler SM, Tyrrell PN, Harvey E, Hebert D, Silverman ED (2009) Ethnic differences in pediatric systemic lupus erythematosus. J Rheumatol 36:2539–2546

    Article  PubMed  Google Scholar 

  12. Lewandowski LB, Schanberg LE, Thielman N, Phuti A, Kalla AA, Okpechi I, Nourse P, Gajjar P, Faller G, Ambaram P, Reuter H, Spittal G, Scott C (2017) Severe disease presentation and poor outcomes among pediatric systemic lupus erythematosus patients in South Africa. Lupus 26:186–194

    Article  CAS  PubMed  Google Scholar 

  13. Miguel DF, Terreri MT, Pereira RMR, Bonfa E, Silva CAA, Corrente JE, Magalhaes CS, Brazilian Childhood-onset Systemic Lupus Erythematosus Group (2020) Comparison of urinary parameters, biomarkers, and outcome of childhood systemic lupus erythematosus early onset-lupus nephritis. Adv Rheumatol 60:10

    Article  PubMed  Google Scholar 

  14. Tang SP, Lim SC, Arkachaisri T (2021) Childhood-onset systemic lupus erythematosus: Southeast Asian perspectives. J Clin Med 10:559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Tan JH, Hoh SF, Win MT, Chan YH, Das L, Arkachaisri T (2015) Childhood-onset systemic lupus erythematosus in Singapore: clinical phenotypes, disease activity, damage, and autoantibody profiles. Lupus 24:998–1005

    Article  CAS  PubMed  Google Scholar 

  16. Abujam B, Gupta A, Suri D, Rawat A, Singh S (2016) Trends and predictors of mortality in childhood onset lupus in a single North-Indian centre over 23 years: a retrospective study. Clin Exp Rheumatol 34:554–559

    PubMed  Google Scholar 

  17. Rubinstein TB, Knight AM (2020) Disparities in childhood-onset lupus. Rheum Dis Clin North Am 46:661–672

    Article  PubMed  Google Scholar 

  18. Bakr A (2005) Epidemiology treatment and outcome of childhood systemic lupus erythematosus in Egypt. Pediatr Nephrol 20:1081–1086

    Article  PubMed  Google Scholar 

  19. Rullo OJ, McCurdy DK, Yadin O, Hoftman ADC, Woo JMP, von Scheven E, CARRAnet Investigators (2011) Race, ethnicity and gender affect the severity of renal outcomes in patients with pediatric systemic lupus erythematosus: an analysis of the CARRAnet data at baseline visit. Arthritis Rheumatol 63:S781–S782

    Google Scholar 

  20. Isenberg D, Appel GB, Contreras G, Dooley MA, Ginzler EM, Jayne D, Sanchez-Guerrero J, Wofsy D, Yu X, Solomons N (2010) Influence of race/ethnicity on response to lupus nephritis treatment: the ALMS study. Rheumatology (Oxford) 49:128–140

    Article  PubMed  Google Scholar 

  21. Yap DY, Chan TM (2015) Lupus nephritis in Asia: clinical features and management. Kidney Dis (Basel) 1:100–109

    Article  PubMed  Google Scholar 

  22. Charras A, Smith E, Hedrich CM (2021) Systemic lupus erythematosus in children and young people. Curr Rheumatol Rep 23:20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Hanscombe KB, Morris DL, Noble JA, Dilthey AT, Tombleson P, Kaufman KM, Comeau M, Langefeld CD, Alarcon-Riquelme ME, Gaffney PM, Jacob CO, Sivils KL, Tsao BP, Alarcon GS, Brown EE, Croker J, Edberg J, Gilkeson G, James JA, Kamen DL, Kelly JA, McCune J, Merrill JT, Petri M, Ramsey-Goldman R, Reveille JD, Salmon JE, Scofield H, Utset T, Wallace DJ, Weisman MH, Kimberly RP, Harley JB, Lewis CM, Criswell LA, Vyse TJ (2018) Genetic fine mapping of systemic lupus erythematosus MHC associations in Europeans and African Americans. Hum Mol Genet 27:3813–3824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Lanata CM, Paranjpe I, Nititham J, Taylor KE, Gianfrancesco M, Paranjpe M, Andrews S, Chung SA, Rhead B, Barcellos LF, Trupin L, Katz P, Dall’Era M, Yazdany J, Sirota M, Criswell LA (2019) A phenotypic and genomics approach in a multi-ethnic cohort to subtype systemic lupus erythematosus. Nat Commun 10:3902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Peschken CA (2020) Health disparities in systemic lupus erythematosus. Rheum Dis Clin North Am 46:673–683

    Article  PubMed  Google Scholar 

  26. Wilhelmus S, Bajema IM, Bertsias GK, Boumpas DT, Gordon C, Lightstone L, Tesar V, Jayne DR (2016) Lupus nephritis management guidelines compared. Nephrol Dial Transplant 31:904–913

    Article  PubMed  Google Scholar 

  27. Oni L, Wright RD, Marks S, Beresford MW, Tullus K (2021) Kidney outcomes for children with lupus nephritis. Pediatr Nephrol 36:1377–1385

    Article  PubMed  Google Scholar 

  28. 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, Carra SLE Subcommittee (2012) Consensus treatment plans for induction therapy of newly diagnosed proliferative lupus nephritis in juvenile systemic lupus erythematosus. Arthritis Care Res (Hoboken) 64:375–383

  29. Kidney Disease: Improving Global Outcomes Glomerular Diseases Work Group (2021) KDIGO 2021 clinical practice guideline for the management of glomerular diseases. Kidney Int 100:S1–S276

    Article  Google Scholar 

  30. De Mutiis C, Wenderfer SE, Orjuela A, Bagga A, Basu B, Sar T, Aggarwal A, Jain A, Yap HK, Ito S, Ohnishi A, Iwata N, Kasapcopur O, Laurent A, Mastrangelo A, Ogura M, Shima Y, Rianthavorn P, Silva CA, Trindade V, Dormi A, Tullus K (2021) Defining renal remission in an international cohort of 248 children and adolescents with lupus nephritis. Rheumatology (Oxford) 61:2563–2571

    Article  Google Scholar 

  31. Chen L, Tan M, Huang J, Wen S, Cheng C, Liu Y, Li B, Chen W, Peng S, Yu Z, Li Y, Jiang X (2021) Effects of alternative remission criteria on outcome of pediatric proliferative lupus nephritis: a multi-center retrospective study of pediatric proliferative lupus nephritis. Am J Transl Res 13:4510–4520

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Hugle B, Silverman ED, Tyrrell PN, Harvey EA, Hebert D, Benseler SM (2015) Presentation and outcome of paediatric membranous non-proliferative lupus nephritis. Pediatr Nephrol 30:113–121

    Article  PubMed  Google Scholar 

  33. Abdulrahman MA, Sallam DE (2020) Treatment response and progression to end stage renal disease in adolescents and young adults with lupus nephritis: a follow up study in an Egyptian cohort. The Egyptian Rheumatologist 42:189–193

    Article  Google Scholar 

  34. Zhang CX, Cai L, Zhou ZY, Mao YY, Huang H, Yin L, Chen TX, Zhou W (2019) Clinical manifestations, immunological features and prognosis of Chinese pediatric systemic lupus erythematosus: a single-center study. Int J Rheum Dis 22:1070–1076

    CAS  PubMed  Google Scholar 

  35. Hui M, Garner R, Rees F, Bavakunji R, Daniel P, Varughese S, Srikanth A, Andres M, Pearce F, Leung J, Lim K, Regan M, Lanyon P (2013) Lupus nephritis: a 15-year multi-centre experience in the UK. Lupus 22:328–332

    Article  CAS  PubMed  Google Scholar 

  36. Tektonidou MG, Dasgupta A, Ward MM (2016) Risk of end-stage renal disease in patients with lupus nephritis, 1971–2015: a systematic review and Bayesian meta-analysis. Arthritis Rheumatol 68:1432–1441

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Wu XY, Yang M, Xie YS, Xiao WG, Lin J, Zhou B, Guan X, Luo CN, Che N, Liu XZ, Wang C, Teng JL, Cheng XB, Ye JN, Su YT, Shi H, Yin YF, Liu MR, Sun Y, Hu QY, Zhou ZC, Chi HH, Liu Y, Zhang X, Chen JW, Zhang MJ, Zhao DB, Yang CD, Wu LJ, Liu HL (2019) Causes of death in hospitalized patients with systemic lupus erythematosus: a 10-year multicenter nationwide Chinese cohort. Clin Rheumatol 38:107–115

    Article  PubMed  Google Scholar 

  39. Hari P, Bagga A, Mahajan P, Dinda A (2009) Outcome of lupus nephritis in Indian children. Lupus 18:348–354

    Article  CAS  PubMed  Google Scholar 

  40. Srivastava P, Abujam B, Misra R, Lawrence A, Agarwal V, Aggarwal A (2016) Outcome of lupus nephritis in childhood onset SLE in North and Central India: single-centre experience over 25 years. Lupus 25:547–557

    Article  CAS  PubMed  Google Scholar 

  41. 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 

  42. Tektonidou MG, Lewandowski LB, Hu J, Dasgupta A, Ward MM (2017) Survival in adults and children with systemic lupus erythematosus: a systematic review and Bayesian meta-analysis of studies from 1950 to 2016. Ann Rheum Dis 76:2009–2016

    Article  PubMed  Google Scholar 

  43. Emre S, Bilge I, Sirin A, Kilicaslan I, Nayir A, Oktem F, Uysal V (2001) Lupus nephritis in children: prognostic significance of clinicopathological findings. Nephron 87:118–126

    Article  CAS  PubMed  Google Scholar 

  44. 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 

  45. 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 

  46. Al-Mayouf SM, AlAmeer A, Alfattani A, Alsonbul A (2017) Outcome of childhood lupus nephritis in Saudi children. Saudi J Kidney Dis Transpl 28:1015–1020

    Article  PubMed  Google Scholar 

  47. Al Hamzi H, Alhaymouni B, Al Shaikh A, Al-Mayouf SM (2014) Outcome of adult Saudi patients with childhood-onset systemic lupus erythematosus. Clin Exp Rheumatol 32:984–988

    PubMed  Google Scholar 

  48. Groot N, Shaikhani D, Teng YKO, de Leeuw K, Bijl M, Dolhain R, Zirkzee E, Fritsch-Stork R, Bultink IEM, Kamphuis S (2019) Long-term clinical outcomes in a cohort of adults with childhood-onset systemic lupus erythematosus. Arthritis Rheumatol 71:290–301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. 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 

  50. Demir S, Gülhan B, Özen S, Çeleğen K, Batu ED, Taş N, Orhan D, Bilginer Y, Düzova A, Ozaltin F, Topaloğlu R (2021) Long term renal survival of pediatric patients with lupus nephritis. Nephrol Dial Transplant 37:1069–1077. https://doi.org/10.1093/ndt/gfab152

    Article  CAS  Google Scholar 

  51. 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 

  52. Ruggiero B, Vivarelli M, Gianviti A, Benetti E, Peruzzi L, Barbano G, Corona F, Ventura G, Pecoraro C, Murer L, Ghiggeri GM, Pennesi M, Edefonti A, Coppo R, Emma F (2013) Lupus nephritis in children and adolescents: results of the Italian Collaborative Study. Nephrol Dial Transplant 28:1487–1496

    Article  CAS  PubMed  Google Scholar 

  53. 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 

  54. Hobbs DJ, Barletta GM, Rajpal JS, Rajpal MN, Weismantel DP, Birmingham JD, Bunchman TE (2010) Severe paediatric systemic lupus erythematosus nephritis–a single-centre experience. Nephrol Dial Transplant 25:457–463

    Article  CAS  PubMed  Google Scholar 

  55. 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 

  56. Pattaragarn A, Sumboonnanonda A, Parichatikanond P, Supavekin S, Suntornpoch V, Vongjirad A (2005) Systemic lupus erythematosus in Thai children: clinicopathologic findings and outcome in 82 patients. J Med Assoc Thai 88(Suppl 8):S232-241

    PubMed  Google Scholar 

  57. 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 32:2283–2291

    Article  PubMed  Google Scholar 

  58. Boneparth A, Wenderfer SE, Moorthy LN, Radhakrishna SM, Sagcal-Gironella AC, von Scheven E, CARRA Registry Investigators (2017) Clinical characteristics of children with membranous lupus nephritis: the Childhood Arthritis and Rheumatology Research Alliance Legacy Registry. Lupus 26:299–306

  59. 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 

  60. Wasik H, Chadha V, Galbiati S, Warady B, Atkinson M (2022) Dialysis outcomes for children with lupus nephritis compared to children with other forms of nephritis: a retrospective cohort study. Am J Kidney Dis 79:626–634

    Article  CAS  PubMed  Google Scholar 

  61. Sule S, Fivush B, Neu A, Furth S (2011) Increased risk of death in pediatric and adult patients with ESRD secondary to lupus. Pediatr Nephrol 26:93–98

    Article  PubMed  Google Scholar 

  62. Bacchetta J, Cochat P (2015) Primary disease recurrence-effects on paediatric renal transplantation outcomes. Nat Rev Nephrol 11:371–384

    Article  PubMed  Google Scholar 

  63. Hiraki LT, Feldman CH, Marty FM, Winkelmayer WC, Guan H, Costenbader KH (2017) Serious infection rates among children with systemic lupus erythematosus enrolled in Medicaid. Arthritis Care Res (Hoboken) 69:1620–1626

    Article  PubMed  Google Scholar 

  64. Laoprasopwattana K, Dissaneewate P, Vachvanichsanong P (2009) Fatal infection in children with lupus nephritis treated with intravenous cyclophosphamide. Pediatr Nephrol 24:1337–1343

    Article  PubMed  Google Scholar 

  65. Taheri S, Beiraghdar F (2011) Lupus nephritis in Iranian children: a review of 60 patients. Ren Fail 33:499–505

    Article  PubMed  Google Scholar 

  66. Ponin L, Poomthavorn P, Pirojsakul K, Lerkvaleekul B, Soponkanaporn S, Chitrapazt N, Vilaiyuk S (2022) Long-term growth and final adult height outcome in childhood-onset systemic lupus erythematosus. Pediatr Rheumatol Online J 20:4

    Article  PubMed  PubMed Central  Google Scholar 

  67. Wei Q, Wang W, Dong Y, Zhong L, Song H (2021) Five years follow-up of juvenile lupus nephritis: a single-center retrospective cohort study. Ann Palliat Med 10:7351–7359

    Article  PubMed  Google Scholar 

  68. Quinlan C, Marks SD, Tullus K (2016) Why are kids with lupus at an increased risk of cardiovascular disease? Pediatr Nephrol 31:861–883

    Article  PubMed  Google Scholar 

  69. Lim LSH, Pullenayegum E, Lim L, Gladman D, Feldman B, Silverman E (2017) From childhood to adulthood: the trajectory of damage in patients with juvenile-onset systemic lupus erythematosus. Arthritis Care Res (Hoboken) 69:1627–1635

    Article  PubMed  Google Scholar 

  70. Hersh AO, von Scheven E, Yazdany J, Panopalis P, Trupin L, Julian L, Katz P, Criswell LA, Yelin E (2009) Differences in long-term disease activity and treatment of adult patients with childhood- and adult-onset systemic lupus erythematosus. Arthritis Rheum 61:13–20

    Article  PubMed  PubMed Central  Google Scholar 

  71. 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 

  72. Oni L, Beresford MW, Witte D, Chatzitolios A, Sebire N, Abulaban K, Shukla R, Ying J, Brunner HI (2017) Inter-observer variability of the histological classification of lupus glomerulonephritis in children. Lupus 26:1205–1211

    Article  CAS  PubMed  Google Scholar 

  73. Bertsias GK, Tektonidou M, Amoura Z, Aringer M, Bajema I, Berden JH, Boletis J, Cervera R, Dorner T, Doria A, Ferrario F, Floege J, Houssiau FA, Ioannidis JP, Isenberg DA, Kallenberg CG, Lightstone L, Marks SD, Martini A, Moroni G, Neumann I, Praga M, Schneider M, Starra A, Tesar V, Vasconcelos C, van Vollenhoven RF, Zakharova H, Haubitz M, Gordon C, Jayne D, Boumpas DT, European League Against Rheumatism and European Renal Association-European Dialysis and Transplant Association (2012) 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 71:1771–1782

  74. Chalhoub NE, Wenderfer SE, Levy DM, Rouster-Stevens K, Aggarwal A, Savani SI, Ruth NM, Arkachaisri T, Qiu T, Merritt A, Onel K, Goilav B, Khubchandani RP, Deng J, Fonseca AR, Ardoin SP, Ciurtin C, Kasapcopur O, Jelusic M, Huber AM, Ozen S, Klein-Gitelman MS, Appenzeller S, Cavalcanti A, Fotis L, Lim SC, Silva RM, Miramontes JR, Rosenwasser NL, Saad-Magalhaes C, Schonenberg-Meinema D, Scott C, Silva CA, Enciso S, Terreri MT, Torres-Jimenez AR, Trachana M, Al-Mayouf SM, Devarajan P, Huang B, Brunner HI, Childhood Arthritis and Rheumatology Research Alliance Lupus Nephritis Work Group and the Pediatric Rheumatology European Society Lupus Working Party (2022) International consensus for the dosing of corticosteroids in childhood-onset systemic lupus erythematosus with proliferative lupus nephritis. Arthritis Rheumatol 74:263–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Groot N, de Graeff N, Marks SD, Brogan P, Avcin T, Bader-Meunier B, Dolezalova P, Feldman BM, Kone-Paut I, Lahdenne P, McCann L, Ozen S, Pilkington CA, Ravelli A, Royen-Kerkhof AV, Uziel Y, Vastert BJ, Wulffraat NM, Beresford MW, Kamphuis S (2017) European evidence-based recommendations for the diagnosis and treatment of childhood-onset lupus nephritis: the SHARE initiative. Ann Rheum Dis 76:1965–1973

    Article  CAS  PubMed  Google Scholar 

  76. Fanouriakis A, Kostopoulou M, Alunno A, Aringer M, Bajema I, Boletis JN, Cervera R, Doria A, Gordon C, Govoni M, Houssiau F, Jayne D, Kouloumas M, Kuhn A, Larsen JL, Lerstrom K, Moroni G, Mosca M, Schneider M, Smolen JS, Svenungsson E, Tesar V, Tincani A, Troldborg A, van Vollenhoven R, Wenzel J, Bertsias G, Boumpas DT (2019) 2019 update of the EULAR recommendations for the management of systemic lupus erythematosus. Ann Rheum Dis 78:736–745

    Article  CAS  PubMed  Google Scholar 

  77. Houssiau FA, Vasconcelos C, D’Cruz D, Sebastiani GD, de Ramon GE, 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 (2010) 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 

  78. Tunnicliffe DJ, Palmer SC, Henderson L, Masson P, Craig JC, Tong A, Singh-Grewal D, Flanc RS, Roberts MA, Webster AC, Strippoli GF (2018) Immunosuppressive treatment for proliferative lupus nephritis. Cochrane Database Syst Rev 6:CD002922

    PubMed  Google Scholar 

  79. Qiu S, Zhang H, Yu S, Yang Q, Zhang G, Yang H, Li Q, Wang M (2022) Clinical manifestations, prognosis, and treat-to-target assessment of pediatric lupus nephritis. Pediatr Nephrol 37:367–376

    Article  PubMed  Google Scholar 

  80. Elmougy A, Sarhan A, Hammad A, El-Refaey A, Zedan M, Eid R, Laimon W, Elrahman AA, Elhussieni F, El-Sherbeny E, Bakr A (2015) Lupus nephritis in Egyptian children: a 16-year experience. J Nephrol 28:557–562

    Article  CAS  PubMed  Google Scholar 

  81. Palmer SC, Tunnicliffe DJ, Singh-Grewal D, Mavridis D, Tonelli M, Johnson DW, Craig JC, Tong A, Strippoli GFM (2017) Induction and maintenance immunosuppression treatment of proliferative lupus nephritis: a network meta-analysis of randomized trials. Am J Kidney Dis 70:324–336

    Article  PubMed  Google Scholar 

  82. Shin JI, Li H, Park S, Yang JW, Lee KH, Jo Y, Park S, Oh J, Kim H, An HJ, Jeong G, Jung H, Lee HJ, Kim JS, Nam SW, Koyanagi A, Jacob L, Hwang J, Yon DK, Lee SW, Tizaoui K, Kronbichler A, Kim JH, Smith L (2022) Induction and maintenance treatment of lupus nephritis: a comprehensive review of meta-analyses. J Clin Med 11:343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Aragon E, Chan YH, Ng KH, Lau YW, Tan PH, Yap HK (2010) Good outcomes with mycophenolate-cyclosporine-based induction protocol in children with severe proliferative lupus nephritis. Lupus 19:965–973

    Article  CAS  PubMed  Google Scholar 

  84. 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 

  85. Mao Y, Yin L, Huang H, Zhou Z, Chen T, Zhou W (2019) Addition of cyclosporine/tacrolimus for pediatric relapsed lupus nephritis during mycophenolate mofetil maintenance therapy. J Int Med Res 47:105–113

    Article  CAS  PubMed  Google Scholar 

  86. Basu B, Roy B, Babu BG (2017) Efficacy and safety of rituximab in comparison with common induction therapies in pediatric active lupus nephritis. Pediatr Nephrol 32:1013–1021

    Article  PubMed  Google Scholar 

  87. Hanaoka H, Yamada H, Kiyokawa T, Iida H, Suzuki T, Yamasaki Y, Ooka S, Nagafuchi H, Okazaki T, Ichikawa D, Shirai S, Shibagaki Y, Koike J, Ozaki S (2017) Lack of partial renal response by 12 weeks after induction therapy predicts poor renal response and systemic damage accrual in lupus nephritis class III or IV. Arthritis Res Ther 19:4

    Article  PubMed  PubMed Central  Google Scholar 

  88. Felsenstein S, Reiff AO, Ramanathan A (2015) Transition of care and health-related outcomes in pediatric-onset systemic lupus erythematosus. Arthritis Care Res (Hoboken) 67:1521–1528

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Arvind Bagga.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khandelwal, P., Govindarajan, S. & Bagga, A. Management and outcomes in children with lupus nephritis in the developing countries. Pediatr Nephrol 38, 987–1000 (2023). https://doi.org/10.1007/s00467-022-05769-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00467-022-05769-x

Keywords

Navigation