Juvenile systemic lupus erythematosus: a single-center experience from southern Turkey

  • Sibel BalciEmail author
  • Rabia Miray Kisla Ekinci
  • Aysun Karabay Bayazit
  • Engin Melek
  • Dilek Dogruel
  • Derya Ufuk Altintas
  • Mustafa Yilmaz
Original Article



This study was conducted to analyze clinical characteristics, laboratory data, disease activity, and outcome of juvenile systemic lupus erythematosus (jSLE) patients from southern Turkey.


Fifty-three patients with jSLE diagnosed according to the revised American College of Rheumatology 1997 criteria between January 2005 and June 2018 were included in the present study.


The median age at the diagnosis was 12.8 (range, 5.1–17.7) years. The female to male ratio was 9.6:1. The most prevalent clinical features were mucocutaneous involvement (96.2%) and constitutional manifestations (94.3%). Renal manifestations, hematological manifestations, and neuropsychiatric involvement were detected in 40 (75%), in 38 (71.7%), and in 13 (24.5%) patients, respectively. Renal biopsy was performed to 49 patients (92.5%). Class IV lupus nephritis (LN) (34%) and class II LN (20.4%) were the most common findings. Mycophenolate mofetil, cyclophosphamide with corticosteroid were the main treatment options. Eighteen patients received rituximab and one tocilizumab. The mean SLE Disease Activity Index (SLEDAI) score at the time of diagnosis was 22.47 ± 8.8 (range = 3–49), and 1.34 ± 1.85 (range = 0–7) at last visit. Twenty-one patients (39.6%) had damage in agreement with Systemic Lupus International Collaborating Clinics/American College of Rheumatology Damage Index (PedSDI; mean = 0.60 ± 0.94; range = 0–5) criteria. Growth failure was the most prevalent cause of damage (n = 13, 26%). One patient deceased due to severe pulmonary hemorrhage and multiple cerebral thromboses.


jSLE patients in this cohort have severe disease in view of the higher frequency of renal and neurologic involvement. Nevertheless, multicenter studies are needed to make a conclusion for all Turkish children with jSLE.


Juvenile systemic lupus erythematosus Lupus nephritis Outcome Tocilizumab 


Authors’ contributions

Dr. Balci and Dr. Yilmaz conceptualized and designed the study, drafted the initial manuscript, and reviewed and revised the manuscript. Dr. Kişla Ekinci, Dr.Karabay Bayazit, Dr. Melek, and Dr. Dogruel collected data, carried out the initial analyses, and reviewed and revised the manuscript. Dr. Altintas and Dr. Dogruel designed the data collection instruments, coordinated and supervised data collection, and critically reviewed the manuscript. All authors approved the final manuscript as submitted and agree to be accountable for all aspects of the work.


No funding was received.

Compliance with ethical standards



Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Approval of the institutional review board of the local medical school was obtained.

Informed consent

Written informed consent was obtained from all patients or their legal guardians according to legal ethics regulations.


  1. 1.
    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. CrossRefGoogle Scholar
  2. 2.
    Danchenko N, Satia JA, Anthony MS (2006) Epidemiology of systemic lupus erythematosus: a comparison of worldwide disease burden. Lupus 15:308–318. CrossRefGoogle Scholar
  3. 3.
    Pineles D, Valente A, Warren B, Peterson MG, Lehman TJ, Moorthy LN (2011) Worldwide incidence and prevalence of pediatric onset systemic lupus erythematosus. Lupus 20:1187–1192. CrossRefGoogle Scholar
  4. 4.
    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. CrossRefGoogle Scholar
  5. 5.
    Kamphuis S, Silverman ED (2010) Prevalence and burden of pediatric-onset systemic lupus erythematosus. Nat Rev Rheumatol 6:538–546. CrossRefGoogle Scholar
  6. 6.
    Borchers AT, Naguwa SM, Shoenfeld Y, Gershwin ME (2010) The geoepidemiology of systemic lupus erythematosus. Autoimmun Rev 9:A277–A287. CrossRefGoogle Scholar
  7. 7.
    Artim-Esen B, Şahin S, Çene E, Şahinkaya Y, Barut K, Adrovic A, Özlük Y, Kılıçaslan I, Omma A, Gül A, Öcal L, Kasapçopur Ö, İnanç M (2017) Comparison of disease characteristics, organ damage, and survival in patients with juvenile-onset and adult-onset systemic lupus erythematosus in a combined cohort from 2 tertiary centers in Turkey. J Rheumatol 44:619–625. CrossRefGoogle Scholar
  8. 8.
    Sahin S, Adrovic A, Barut K, Canpolat N, Ozluk Y, Kilicaslan I, Caliskan S, Sever L, Kasapcopur O (2018) Juvenile systemic lupus erythematosus in Turkey: demographic, clinical and laboratory features with disease activity and outcome. Lupus 27:514–519. CrossRefGoogle Scholar
  9. 9.
    Pejchinovski M, Siwy J, Mullen W, Mischak H, Petri MA, Burkly LC, Wei R (2018) Urine peptidomic biomarkers for diagnosis of patients with systematic lupus erythematosus. Lupus 27:6–16. CrossRefGoogle Scholar
  10. 10.
    Groot N, de Graeff N, Avcin T, Bader-Meunier B, Brogan P, Dolezalova P, Feldman B, Kone-Paut I, Lahdenne P, Marks SD, McCann L, Ozen S, Pilkington C, Ravelli A, Royen-Kerkhof AV, Uziel Y, Vastert B, Wulffraat N, Kamphuis S, Beresford MW (2017) European evidence-based recommendations for diagnosis and treatment of childhood-onset systemic lupus erythematosus: the SHARE initiative. Ann Rheum Dis 76:1788–1796. CrossRefGoogle Scholar
  11. 11.
    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, Özen 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 0:1–9. Google Scholar
  12. 12.
    Hochberg MC (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 40:1725.<1725::AID-ART29>3.0.CO;2-Y CrossRefGoogle Scholar
  13. 13.
    The American College of Rheumatology. Nomenclature and case definitions for neuropsychiatric lupus syndromes Arthritis Rheum 1999; 42: 599–608.<599::AID-ANR2>3.0.CO;2-F.
  14. 14.
    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. CrossRefGoogle Scholar
  15. 15.
    Gladman DD, Ibanez D, Urowitz MB (2002) Systemic lupus erythematosus disease activity index 2000. J Rheumatol 29:288–291Google Scholar
  16. 16.
    Gutiérrez-Suárez 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. CrossRefGoogle Scholar
  17. 17.
    Ambrose N, Morgan TA, Galloway J, Ionnoau Y, Beresford MW, Isenberg DA, UK JSLE Study Group (2016) Differences in disease phenotype and severity in SLE across age groups. Lupus 25:1542–1550. CrossRefGoogle Scholar
  18. 18.
    Hoffman IE, Lauwerys BR, De Keyser F, Huizinga TW, Isenberg D, Cebecauer L, Dehoorne J, Joos R, Hendrickx G, Houssiau F, Elewaut D (2009) Juvenile-onset systemic lupus erythematosus: different clinical and serological pattern than adult-onset systemic lupus erythematosus. Ann Rheum Dis 68:412–415. CrossRefGoogle Scholar
  19. 19.
    Borba EF, Araujo DB, Bonfa´ E, Shinjo SK (2013) Clinical and immunological features of 888 Brazilian systemic lupus patients from a monocentric cohort: comparison with other populations. Lupus 22:744–749. CrossRefGoogle Scholar
  20. 20.
    Gulay CB, Dans LF (2011) Clinical presentations and outcomes of Filipino juvenile systemic lupus erythematosus. Pediatr Rheumatol Online J 9:7. CrossRefGoogle Scholar
  21. 21.
    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. CrossRefGoogle Scholar
  22. 22.
    Bader-Meunier B, Armengaud JB, Haddad E, Salomon R, Deschênes G, Koné-Paut I, Leblanc T, Loirat C, Niaudet P, Piette JC, Prieur AM, Quartier P, Bouissou F, Foulard M, Leverger G, Lemelle I, Pilet P, Rodière M, Sirvent N, Cochat P (2005) Initial presentation of childhood-onset systemic lupus erythematosus: a French multicenter study. J Pediatr 146:648–653. CrossRefGoogle Scholar
  23. 23.
    Adelowo OO, Olaosebikan BH, Animashaun BA, Akintayo RO (2017) Juvenile systemic lupus erythematosus in Nigeria. Lupus 26:329–333. CrossRefGoogle Scholar
  24. 24.
    Abdel-Hafez MA, Abdel-Nabi H (2015) Juvenile systemic lupus erythematosus: onset patterns and short-term outcome in Egyptian children, a single-center experience. Lupus 24:1455–1461. CrossRefGoogle Scholar
  25. 25.
    Concannon A, Rudge S, Yan J, Reed P (2013) The incidence, diagnostic clinical manifestations and severity of juvenile systemic lupus erythematosus in New Zealand Maori and Pacific Island children: the starship experience (2000–2010). Lupus 22:1156–1161. CrossRefGoogle Scholar
  26. 26.
    Abdel-Nabi HH, Abdel-Noor RA (2018) Comparison between disease onset patterns of Egyptian juvenile and adult systemic lupus erythematosus (single Centre experience). Lupus 27:1039–1044. CrossRefGoogle Scholar
  27. 27.
    Dung NT, Loan HT, Nielsen S, Zak M, Petersen FK (2012) Juvenile systemic lupus erythematosus onset patterns in Vietnamese children: a descriptive study of 45 children. Pediatr Rheumatol Online J 10:38. CrossRefGoogle Scholar
  28. 28.
    Couture J, Silverman ED (2016) Update on the pathogenesis and treatment of childhood-onset systemic lupus erythematosus. Curr Opin Rheumatol 28:488–496. CrossRefGoogle Scholar
  29. 29.
    Pluchinotta FR, Schiavo B, Vittadello F, Martini G, Perilongo G, Zulian F (2007) Distinctive clinical features of pediatric systemic lupus erythematosus in three different age classes. Lupus 16:550–555. CrossRefGoogle Scholar
  30. 30.
    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 Thail 8:232–241Google Scholar
  31. 31.
    Ramírez Gómez LA, Uribe Uribe O, Osio Uribe O et al (2008) Childhood systemic lupus erythematosus in Latin America. The GLADEL experience in 230 children. Lupus 1:596–604. CrossRefGoogle Scholar
  32. 32.
    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. CrossRefGoogle Scholar
  33. 33.
    Tanaka T, Narazaki M, Kishimoto T (2014) IL-6 in inflammation, immunity, and disease. Cold Spring Harb Perspect Biol 4 6:a016295. CrossRefGoogle Scholar
  34. 34.
    Tackey E, Lipsky PE, Illei GG (2004) Rationale for interleukin-6 blockade in systemic lupus erythematosus. Lupus 13:339–343. CrossRefGoogle Scholar
  35. 35.
    Kamata Y, Minota S (2012) Successful treatment of massive intractable pericardial effusion in a patient with systemic lupus erythematosus with tocilizumab. BMJ Case Rep 21:2012. Google Scholar
  36. 36.
    Ocampo V, Haaland D, Legault K, Mittoo S, Aitken E (2016) Successful treatment of recurrent pleural and pericardial effusions with tocilizumab in a patient with systemic lupus erythematous. BMJ Case Rep 8:2016. Google Scholar
  37. 37.
    Cavalcante EG, Aikawa NE, Lozano RG, Lotito AP, Jesus AA, Silva CA (2011) Chronic polyarthritis as the first manifestation of juvenile systemic lupus erythematosus patients. Lupus 20:960–964. CrossRefGoogle Scholar
  38. 38.
    Brunner HI, Higgins GC, Wiers K, Lapidus SK, Olson JC, Onel K, Punaro M, Ying J, Klein-Gitelman MS, Seid M (2009) Health-related quality of life and its relationship to patient disease course in childhood-onset systemic lupus erythematosus. J Rheumatol 36:1536–1545. CrossRefGoogle Scholar
  39. 39.
    Alarcón-Segovia D, Alarcón-Riquelme ME, Cardiel MH, Caeiro F, Massardo L, Villa AR, Pons-Estel BA, on behalf of the Grupo Latinoamericano de Estudio del Lupus Eritematoso (GLADEL) (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. CrossRefGoogle Scholar
  40. 40.
    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.
  41. 41.
    Al Arfaj AS, Khalil N (2009) Clinical and immunological manifestations in 624 SLE patients in Saudi Arabia. Lupus 18:465–473. CrossRefGoogle Scholar
  42. 42.
    Araujo DB, Borba EF, Silva CA, Campos LM, Pereira RM, Bonfa E, Shinjo SK (2012) Alveolar hemorrhage: distinct features of juvenile and adult onset systemic lupus erythematosus. Lupus 21:872–877. CrossRefGoogle Scholar
  43. 43.
    Martinez-Martinez MU, Abud-Mendoza C (2014) Diffuse alveolar hemorrhage in patients with systemic lupus erythematosus. Clinical manifestations, treatment, and prognosis. Reumatol Clin 10:248–253. CrossRefGoogle Scholar
  44. 44.
    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. CrossRefGoogle Scholar
  45. 45.
    Al-Mayouf SM (2013) Systemic lupus erythematosus in Saudi children: long-term outcomes. Int J Rheum Dis 16:56–60. CrossRefGoogle Scholar

Copyright information

© International League of Associations for Rheumatology (ILAR) 2019

Authors and Affiliations

  1. 1.Department of Pediatric Rheumatology, Faculty of MedicineCukurova UniversityAdanaTurkey
  2. 2.Department of Pediatric Nephrology, Faculty of MedicineCukurova UniversityAdanaTurkey
  3. 3.Department of Pediatric Allergy and Immunology, Faculty of MedicineCukurova UniversityAdanaTurkey

Personalised recommendations