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Gastrointestinal system manifestations in juvenile systemic lupus erythematosus

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Abstract

Systemic lupus erythematosus (SLE) is an autoimmune disease which may involve gastrointestinal system (GIS). The aim of this study was to present GIS manifestations of pediatric SLE patients. The medical files of 69 children with SLE followed between January 2011 and January 2016 were reviewed. All fulfilled the Systemic Lupus International Collaborating Clinics criteria. All patients (≤18 years of age) with GIS manifestations were included. GIS manifestations were observed in 19 (27.5%) out of 69 SLE patients and present at the time of SLE diagnosis in 13 (68.4%). The GIS manifestations due to SLE were autoimmune hepatitis (AIH) (n = 8) and lupus enteritis (n = 1). Manifestations associated with SLE were hepatomegaly and hypertransaminasemia due to macrophage activation syndrome (MAS) (n = 3) and hepatic steatosis (n = 1). GIS manifestations as a result of the adverse events of drugs were as follows: toxic hepatitis (n = 3; associated with methotrexate and nonsteroidal anti-inflammatory drugs in one, methotrexate in another, and azathioprine in another patient), azathioprine-induced cholestatic hepatitis (n = 1), and gastritis associated with corticosteroid (n = 1). In one patient, acute appendicitis occurred as a coincidence. In this study, one of every five pediatric SLE patients had GIS-related manifestations. GIS involvement may occur as an initial manifestation of the disease.

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References

  1. Tucker LB, Menon S, Schaller JG, Isenberg DA (1995) Adult- and childhood-onset systemic lupus erythematosus: a comparison of onset, clinical features, serology, and outcome. Br J Rheumatol 34:866–872

    Article  CAS  PubMed  Google Scholar 

  2. Malattia C, Martini A (2013) Paediatric-onset systemic lupus erythematosus. Best Pract Res Clin Rheumatol 27:351–362. doi:10.1016/j.berh.2013.07.007

    Article  PubMed  Google Scholar 

  3. 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. doi:10.1177/0961203314563817

    Article  CAS  PubMed  Google Scholar 

  4. Hallegua DS, Wallace DJ (2000) Gastrointestinal manifestations of systemic lupus erythematosus. Curr Opin Rheumatol 12:379–385

    Article  CAS  PubMed  Google Scholar 

  5. Ebert EC, Hagspiel KD (2011) Gastrointestinal and hepatic manifestations of systemic lupus erythematosus. J Clin Gastroenterol 45:436–441. doi:10.1097/MCG.0b013e31820f81b8

    Article  CAS  PubMed  Google Scholar 

  6. Bader-Meunier B, Armengaud JB, Haddad E et al (2005) Initial presentation of childhood-onset systemic lupus erythematosus: a French multicenter study. J Pediatric 146:648–653

    Article  CAS  Google Scholar 

  7. Mok CC (2005) Investigations and management of gastrointestinal and hepatic manifestations of systemic lupus erythematosus. Best Pract Res Clin Rheumatol 19:741–766

    Article  CAS  PubMed  Google Scholar 

  8. Sultan SM, Ioannou Y, Isenberg DA (1999) A review of gastrointestinal manifestations of systemic lupus erythematosus. Rheumatology (Oxford) 38:917–932

    Article  CAS  Google Scholar 

  9. Pistiner M, Wallace DJ, Nessim S, Metzger AL, Klinenberg JR (1991) Lupus erythematosus in the 1980s: a survey of 570 patients. Semin Arthritis Rheum 21:55–64

    Article  CAS  PubMed  Google Scholar 

  10. Tu YL, Yeh KW, Chen LC, Yao TC, Ou LS, Lee WI, Huang JL (2011) Differences in disease features between childhood-onset and adult-onset systemic lupus erythematosus patients presenting with acute abdominal pain. Semin Arthritis Rheum 40:447–454

    Article  PubMed  Google Scholar 

  11. Huggins JL, Holland MJ, Brunner HI (2016) Organ involvement other than lupus nephritis in childhood-onset systemic lupus erythematosus. Lupus 25:857–863. doi:10.1177/0961203316644339

    Article  CAS  PubMed  Google Scholar 

  12. Petri M, Orbai AM, Alarcon GS, Gordon C et al (2012) Derivation and validation of the Systemic Lupus International Collaborating Clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum 64:2677–2686. doi:10.1002/art.34473

    Article  PubMed  PubMed Central  Google Scholar 

  13. Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH (1992) Derivation of the SLEDAI. A disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. Arthritis Rheum 35:630–640

    Article  CAS  PubMed  Google Scholar 

  14. Liberal R, Vergani D, Mieli-Vergani G (2015) Update on autoimmune hepatitis. J Clin Transl Hepatol 3(1):42–52 doi:10.14218/JCTH.2014.00032

  15. Leise MD, Poterucha JJ, Talwalkar JA (2014) Drug-induced liver injury. Mayo Clin Proc 89:95–106. doi:10.1016/j.mayocp.2013.09.016

    Article  CAS  PubMed  Google Scholar 

  16. Sag E, Tartaglione A, Batu ED, Ravelli A, Khalil SM, Marks SD, Ozen S (2014) Performance of the new SLICC classification criteria in childhood systemic lupus erythematosus: a multicentre study. Clin Exp Rheumatol 32:440–444

    CAS  PubMed  Google Scholar 

  17. Carreno L, Lopez-Longo FJ, Monteagudo I, Rodriguez-Mahou M, Bascones M, Gonzalez CM, Saint-Cyr C, Lapointe N (1999) Immunological and clinical differences between juvenile and adult onset of systemic lupus erythematosus. Lupus 8:287–292

    Article  CAS  PubMed  Google Scholar 

  18. Choi JH, Park DJ, Kang JH et al (2015) Comparison of clinical and serological differences among juvenile-, adult-, and late-onset systemic lupus erythematosus in Korean patients. Lupus 24:1342–1349. doi:10.1177/0961203315591024

    Article  CAS  PubMed  Google Scholar 

  19. Descloux E, Durieu I, Cochat P, Vital-Durand D, Ninet J, Fabien N, Cimaz R (2009) Influence of age at disease onset in the outcome of paediatric systemic lupus erythematosus. Rheumatology (Oxford) 48:779–784. doi:10.1093/rheumatology/kep067

    Article  Google Scholar 

  20. Hoffman IE, Lauwerys BR, De Keyser F et al (2009) Juvenile-onset systemic lupus erythematosus: different clinical and serological pattern than adult-onset systemic lupus erythematosus. Ann Rheum Dis 68:412–415. doi:10.1136/ard.2008.094813

    Article  CAS  PubMed  Google Scholar 

  21. Richer O, Ulinski T, Lemelle I et al (2007) Abdominal manifestations in childhood-onset systemic lupus erythematosus. Ann Rheum Dis 66:174–178

    Article  CAS  PubMed  Google Scholar 

  22. Fawzy M, Edrees A, Okasha H, El Ashmaui A, Ragab G (2016) Gastrointestinal manifestations in systemic lupus erythematosus. Lupus 25:1456–1462. doi:10.1177/0961203316642308

    Article  CAS  PubMed  Google Scholar 

  23. Longhi MS, Mieli-Vergani G, Vergani D (2014) Autoimmune hepatitis. Curr Pediatr Rev 10:268–274

    Article  CAS  PubMed  Google Scholar 

  24. Liberal R, Grant CR, Longhi MS, Mieli-Vergani G, Vergani D (2014) Diagnostic criteria of autoimmune hepatitis. Autoimmun Rev 13:435–440. doi:10.1016/j.autrev.2013.11.009

    Article  CAS  PubMed  Google Scholar 

  25. Calich AL, Viana VS, Cancado E et al (2013) Anti-ribosomal P protein: a novel antibody in autoimmune hepatitis. Liver Int 33:909–913. doi:10.1111/liv.12155

    Article  PubMed  Google Scholar 

  26. Della Corte C, Sartorelli MR, Sindoni CD, Girolami E, Giovannelli L, Comparcola D, Nobili V (2012) Autoimmune hepatitis in children: an overview of the disease focusing on current therapies. Eur J Gastroenterol Hepatol 24:739–746. doi:10.1097/MEG.0b013e328353750c

    Article  CAS  PubMed  Google Scholar 

  27. Battagliotti C, Rispolo Klubek D, Karakachoff M, Costaguta A (2016) An overlap syndrome involving systemic lupus erythematosus and autoimmune hepatitis in an adolescent girl. Arch Argent Pediatr 2016 114(3):e155–e158. doi:10.5546/aap.2016.eng.e155

    Google Scholar 

  28. Irving KS, Sen D, Tahir H, Pilkington C, Isenberg DA (2007) A comparison of autoimmune liver disease in juvenile and adult populations with systemic lupus erythematosus—a retrospective review of cases. Rheumatology (Oxford) 46:1171–1173

    Article  CAS  Google Scholar 

  29. Bessone F, Poles N, Roma MG (2014) Challenge of liver disease in systemic lupus erythematosus: clues for diagnosis and hints for pathogenesis. World Hepatol 6:394–409. doi:10.4254/wjh.v6.i6.394

    Article  Google Scholar 

  30. Battagliotti C, Rispolo Klubek D, Karakachoff M, Costaguta A (2016) An overlap syndrome involving systemic lupus erythematosus and autoimmune hepatitis in an adolescent girl. Arch Argent Pediatr 114:e155–e158. doi:10.5546/aap.2016.eng.e155

    PubMed  Google Scholar 

  31. Janssens P, Arnaud L, Galicier L, Mathian A, Hie M, Sene D, Haroche J, Veyssier-Belot C, Huynh-Charlier I, Grenier PA et al Lupus enteritis: from clinical findings to therapeutic management. Orphanet J Rare Dis 8:67. doi:10.1186/1750-1172-8-67

  32. Vilaiyuk S, Sirachainan N, Wanitkun S, Pirojsakul K, Vaewpanich J (2013) Recurrent macrophage activation syndrome as the primary manifestation in systemic lupus erythematosus and the benefit of serial ferritin measurements: a case-based review. Clin Rheumatol 32:899–904. doi:10.1007/s10067-013-2227-1

    Article  PubMed  Google Scholar 

  33. Grover S, Rastogi A, Singh J, Rajbongshi A, Bihari C (2014) Spectrum of histomorphologic findings in liver in patients with SLE: a review. Hepat Res Treat 2014:562979. doi:10.1155/2014/562979

    PubMed  PubMed Central  Google Scholar 

  34. Conway R, Low C, Coughlan RJ, O’Donnell MJ, Carey JJ (2015) Risk of liver injury among methotrexate users: a meta-analysis of randomised controlled trials. Semin Arthritis Rheum 45:156–162. doi:10.1016/j.semarthrit.2015.05.003

    Article  CAS  PubMed  Google Scholar 

  35. Chertoff J, Alam S, Black M, Elgendy IY (2014) Azathioprine-induced hepatitis and cholestasis occurring 1 year after treatment. BMJ Case Res. doi:10.1136/bcr-2014-206859

    Google Scholar 

  36. Sood A, Midha V, Sood N, Bansal M (2006) Long term results of use of azathioprine in patients with ulcerative colitis in India. World J Gastroenterol 12:7332–7336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Medina F, Ayala A, Jara LJ, Becerra M, Miranda JM, Fraga A (1997) Acute abdomen in systemic lupus erythematosus: the importance of early laparotomy. Am J Med 103:100–105

    Article  CAS  PubMed  Google Scholar 

  38. Xu D, Yang H, Lai CC, Li P, Zhang X, Yang XO, Zhang FC, Qian JM (2010) Clinical analysis of systemic lupus erythematosus with gastrointestinal manifestations. Lupus 19:866–869. doi:10.1177/0961203310365883

    Article  CAS  PubMed  Google Scholar 

  39. Tian XP, Zhang X (2010) Gastrointestinal involvement in systemic lupus erythematosus: insight into pathogenesis, diagnosis and treatment. World J Gastroenterol 16:2971–2977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Clotet B, Guardia J, Pigrau C, Lience E, Murcia C, Pujol R, Bacardi R (1984) Incidence and clinical significance of anti-ENA antibodies in systemic lupus erythematosus. Estimation by counterimmunoelectrophoresis. Scand J Rheumatol 13:15–20

    Article  CAS  PubMed  Google Scholar 

  41. Alba P, Bento L, Cuadrado MJ, Karim Y, Tungekar MF, Abbs I, Khamashta MA, D’Cruz D, Hughes GR (2003) Anti-dsDNA, anti-Sm antibodies, and the lupus anticoagulant: significant factors associated with lupus nephritis. Ann Rheum Dis 62:556–560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

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Authors and Affiliations

  1. Department of Pediatrics, Division of Rheumatology, Hacettepe University Faculty of Medicine, Sıhhiye, 06100, Ankara, Turkey

    Hafize Emine Sönmez, Ezgi Deniz Batu, Yelda Bilginer & Seza Özen

  2. Department of Pediatrics, Division of Gastroenterology and Hepatology, Hacettepe University Faculty of Medicine, Ankara, Turkey

    Asuman Nur Karhan, Ersin Gümüş, Hülya Demir & Aysel Yüce

Authors
  1. Hafize Emine Sönmez
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  2. Asuman Nur Karhan
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  3. Ezgi Deniz Batu
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  8. Seza Özen
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Correspondence to Seza Özen.

Ethics declarations

The study was approved by the ethics committee of Hacettepe University and was performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki. All these patient files were evaluated retrospectively and all patients were anonymous. When the patients admitted to the hospital, the parents gave a general consent approving anonymous data use for academic purpose.

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Hafize Emine Sönmez and Asuman Nur Karhan contributed equally to the manuscript.

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Sönmez, H.E., Karhan, A.N., Batu, E.D. et al. Gastrointestinal system manifestations in juvenile systemic lupus erythematosus. Clin Rheumatol 36, 1521–1526 (2017). https://doi.org/10.1007/s10067-017-3571-3

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  • DOI: https://doi.org/10.1007/s10067-017-3571-3

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