Macrophage activation syndrome in children with systemic juvenile idiopathic arthritis and systemic lupus erythematosus

Rheumatology International

Volumn 36, Issue 10, 2016, Pages 1421-1429

  Aytaç, Selin ^a   Batu, Ezgi Deniz ^a   Ünal, Şule ^a   Bilginer, Yelda ^a   Çetin, Mualla ^a   Tuncer, Murat ^a   Gümrük, Fatma ^a   Özen, Seza ^a  

^a HACETTEPE UNIVERSITY   (Turkey)

Author keywords

Child; Macrophage activation syndrome; Systemic juvenile idiopathic arthritis; Systemic lupus erythematosus

Indexed keywords

ALANINE AMINOTRANSFERASE; ALBUMIN; ASPARTATE AMINOTRANSFERASE; C REACTIVE PROTEIN; CANAKINUMAB; CORTICOSTEROID; CYANOCOBALAMIN; CYCLOSPORIN A; ETOPOSIDE; FERRITIN; FIBRINOGEN; HEMOGLOBIN; IMMUNOGLOBULIN; LACTATE DEHYDROGENASE; RECOMBINANT INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; TRIACYLGLYCEROL; CYCLOSPORIN; IMMUNOSUPPRESSIVE AGENT;

ADOLESCENT; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ALBUMIN BLOOD LEVEL; ARTHRALGIA; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CHILD; CHILDHOOD MORTALITY; CLINICAL FEATURE; CLINICAL OUTCOME; CONTROLLED STUDY; CORTICOSTEROID THERAPY; DYSPNEA; ERYTHROCYTE SEDIMENTATION RATE; FATIGUE; FEMALE; FERRITIN BLOOD LEVEL; FEVER; FIBRINOGEN BLOOD LEVEL; HEMOGLOBIN BLOOD LEVEL; HEPATOSPLENOMEGALY; HUMAN; HYPERFERRITINEMIA; IMMUNOSUPPRESSIVE TREATMENT; IMMUNOTHERAPY; LACTATE DEHYDROGENASE BLOOD LEVEL; MACROPHAGE ACTIVATION SYNDROME; MAJOR CLINICAL STUDY; MALE; MEDICAL RECORD REVIEW; MORTALITY RATE; ONSET AGE; PARTIAL THROMBOPLASTIN TIME; PERICARDIAL EFFUSION; PLASMAPHERESIS; PLEURA EFFUSION; PRIORITY JOURNAL; RASH; RETROSPECTIVE STUDY; SYSTEMIC JUVENILE IDIOPATHIC ARTHRITIS; SYSTEMIC LUPUS ERYTHEMATOSUS; TRIACYLGLYCEROL BLOOD LEVEL; VITAMIN BLOOD LEVEL; ARTHRITIS, JUVENILE; COMPLICATION; INFANT; LUPUS ERYTHEMATOSUS, SYSTEMIC; PRESCHOOL CHILD; TREATMENT OUTCOME;

ADOLESCENT; ADRENAL CORTEX HORMONES; ARTHRITIS, JUVENILE; CHILD; CHILD, PRESCHOOL; CYCLOSPORINE; FATIGUE; FEMALE; HUMANS; IMMUNOSUPPRESSIVE AGENTS; INFANT; LUPUS ERYTHEMATOSUS, SYSTEMIC; MACROPHAGE ACTIVATION SYNDROME; MALE; RETROSPECTIVE STUDIES; TREATMENT OUTCOME;

EID: 84981225493     PISSN: 01728172     EISSN: 1437160X     Source Type: Journal    
DOI: 10.1007/s00296-016-3545-9     Document Type: Article

References (52)

1. Janka GE (2012) Familial and acquired hemophagocytic lymphohistiocytosis. Annu Rev Med 63:233–246. doi:10.1146/annurev-med-041610-134208
2. Dhote R, Simon J, Papo T, Detournay B, Sailler L, Andre MH, Dupond JL, Larroche C, Piette AM, Mechenstock D, Ziza JM, Arlaud J, Labussiere AS, Desvaux A, Baty V, Blanche P, Schaeffer A, Piette JC, Guillevin L, Boissonnas A, Christoforov B (2003) Reactive hemophagocytic syndrome in adult systemic disease: report of twenty-six cases and literature review. Arthritis Rheum 49:633–639. doi:10.1002/art.11368
3. Rouphael NG, Talati NJ, Vaughan C, Cunningham K, Moreira R, Gould C (2007) Infections associated with haemophagocytic syndrome. Lancet Infect Dis 7:814–822. doi:10.1016/S1473-3099(07)70290-6
4. Stephan JL, Zeller J, Hubert P, Herbelin C, Dayer JM, Prieur AM (1993) Macrophage activation syndrome and rheumatic disease in childhood: a report of four new cases. Clin Exp Rheumatol 11:451–456
5. Lehmberg K, Pink I, Eulenburg C, Beutel K, Maul-Pavicic A, Janka G (2013) Differentiating macrophage activation syndrome in systemic juvenile idiopathic arthritis from other forms of hemophagocytic lymphohistiocytosis. J Pediatr 162:1245–1251. doi:10.1016/j.jpeds.2012.11.081
6. Minoia F, Davi S, Horne A, Demirkaya E, Bovis F, Li C, Lehmberg K, Weitzman S, Insalaco A, Wouters C, Shenoi S, Espada G, Ozen S, Anton J, Khubchandani R, Russo R, Pal P, Kasapcopur O, Miettunen P, Maritsi D, Merino R, Shakoory B, Alessio M, Chasnyk V, Sanner H, Gao YJ, Huasong Z, Kitoh T, Avcin T, Fischbach M, Frosch M, Grom A, Huber A, Jelusic M, Sawhney S, Uziel Y, Ruperto N, Martini A, Cron RQ, Ravelli A, Pediatric Rheumatology International Trials O, Childhood A, Rheumatology Research A, Pediatric Rheumatology Collaborative Study G, Histiocyte S (2014) Clinical features, treatment, and outcome of macrophage activation syndrome complicating systemic juvenile idiopathic arthritis: a multinational, multicenter study of 362 patients. Arthritis Rheumatol 66:3160–3169. doi:10.1002/art.38802
7. Grom AA, Mellins ED (2010) Macrophage activation syndrome: advances towards understanding pathogenesis. Curr Opin Rheumatol 22:561–566. doi:10.1097/01.bor.0000381996.69261.71
8. Ravelli A, Grom AA, Behrens EM, Cron RQ (2012) Macrophage activation syndrome as part of systemic juvenile idiopathic arthritis: diagnosis, genetics, pathophysiology and treatment. Genes Immun 13:289–298. doi:10.1038/gene.2012.3
9. Behrens EM, Canna SW, Slade K, Rao S, Kreiger PA, Paessler M, Kambayashi T, Koretzky GA (2011) Repeated TLR9 stimulation results in macrophage activation syndrome-like disease in mice. J Clin Invest 121:2264–2277. doi:10.1172/JCI43157
10. Strippoli R, Caiello I, De Benedetti F (2013) Reaching the threshold: a multilayer pathogenesis of macrophage activation syndrome. J Rheumatol 40:761–767. doi:10.3899/jrheum.121233
11. Strippoli R, Carvello F, Scianaro R, De Pasquale L, Vivarelli M, Petrini S, Bracci-Laudiero L, De Benedetti F (2012) Amplification of the response to Toll-like receptor ligands by prolonged exposure to interleukin-6 in mice: implication for the pathogenesis of macrophage activation syndrome. Arthritis Rheum 64:1680–1688. doi:10.1002/art.33496
12. Canna SW, Wrobel J, Chu N, Kreiger PA, Paessler M, Behrens EM (2013) Interferon-gamma mediates anemia but is dispensable for fulminant toll-like receptor 9-induced macrophage activation syndrome and hemophagocytosis in mice. Arthritis Rheum 65:1764–1775. doi:10.1002/art.37958
13. Zhang M, Behrens EM, Atkinson TP, Shakoory B, Grom AA, Cron RQ (2014) Genetic defects in cytolysis in macrophage activation syndrome. Curr Rheumatol Rep 16:439. doi:10.1007/s11926-014-0439-2
14. Barut K, Yucel G, Sinoplu AB, Sahin S, Adrovic A, Kasapcopur O (2015) Evaluation of macrophage activation syndrome associated with systemic juvenile idiopathic arthritis: single center experience over a one-year period. Turk Pediatri Ars 50:206–210. doi:10.5152/TurkPediatriArs.2015.3299
15. Bennett TD, Fluchel M, Hersh AO, Hayward KN, Hersh AL, Brogan TV, Srivastava R, Stone BL, Korgenski EK, Mundorff MB, Casper TC, Bratton SL (2012) Macrophage activation syndrome in children with systemic lupus erythematosus and children with juvenile idiopathic arthritis. Arthritis Rheum 64:4135–4142. doi:10.1002/art.34661
16. Yokota S, Imagawa T, Mori M, Miyamae T, Takei S, Iwata N, Umebayashi H, Murata T, Miyoshi M, Tomiita M, Nishimoto N, Kishimoto T (2014) Longterm safety and effectiveness of the anti-interleukin 6 receptor monoclonal antibody tocilizumab in patients with systemic juvenile idiopathic arthritis in Japan. J Rheumatol 41:759–767. doi:10.3899/jrheum.130690
17. Yokota S, Itoh Y, Morio T, Sumitomo N, Daimaru K, Minota S (2015) Macrophage activation syndrome in patients with systemic juvenile idiopathic arthritis under treatment with tocilizumab. J Rheumatol 42:712–722. doi:10.3899/jrheum.140288
18. Zeft A, Hollister R, LaFleur B, Sampath P, Soep J, McNally B, Kunkel G, Schlesinger M, Bohnsack J (2009) Anakinra for systemic juvenile arthritis: the Rocky Mountain Experience. J Clin Rheumatol 15:161–164. doi:10.1097/RHU.0b013e3181a4f459
19. Chiossone L, Audonnet S, Chetaille B, Chasson L, Farnarier C, Berda-Haddad Y, Jordan S, Koszinowski UH, Dalod M, Mazodier K, Novick D, Dinarello CA, Vivier E, Kaplanski G (2012) Protection from inflammatory organ damage in a murine model of hemophagocytic lymphohistiocytosis using treatment with IL-18 binding protein. Front Immunol 3:239. doi:10.3389/fimmu.2012.00239
20. Ohyagi H, Onai N, Sato T, Yotsumoto S, Liu J, Akiba H, Yagita H, Atarashi K, Honda K, Roers A, Muller W, Kurabayashi K, Hosoi-Amaike M, Takahashi N, Hirokawa M, Matsushima K, Sawada K, Ohteki T (2013) Monocyte-derived dendritic cells perform hemophagocytosis to fine-tune excessive immune responses. Immunity 39:584–598. doi:10.1016/j.immuni.2013.06.019
21. Bracaglia CPG, Gatto A, Pardeo M, Lapeyre G, Raganelli L, Marasco E, Insalaco A, Ferlin W, Nelson R, de Min C, De Benedetti F (2015) Anti interferon gamma monoclonal antibody treatment in a child with NLRC4-related disease and severe hemophagocytic lymphohistiocytosis (HLH). Arthritis Rheumatol Suppl 10:67
22. Janka GE, Lehmberg K (2014) Hemophagocytic syndromes–an update. Blood Rev 28:135–142. doi:10.1016/j.blre.2014.03.002
23. Behrens EM, Beukelman T, Paessler M, Cron RQ (2007) Occult macrophage activation syndrome in patients with systemic juvenile idiopathic arthritis. J Rheumatol 34:1133–1138
24. Sawhney S, Woo P, Murray KJ (2001) Macrophage activation syndrome: a potentially fatal complication of rheumatic disorders. Arch Dis Child 85:421–426
25. Stephan JL, Kone-Paut I, Galambrun C, Mouy R, Bader-Meunier B, Prieur AM (2001) Reactive haemophagocytic syndrome in children with inflammatory disorders. A retrospective study of 24 patients. Rheumatology (Oxford) 40:1285–1292
26. Bleesing J, Prada A, Siegel DM, Villanueva J, Olson J, Ilowite NT, Brunner HI, Griffin T, Graham TB, Sherry DD, Passo MH, Ramanan AV, Filipovich A, Grom AA (2007) The diagnostic significance of soluble CD163 and soluble interleukin-2 receptor alpha-chain in macrophage activation syndrome and untreated new-onset systemic juvenile idiopathic arthritis. Arthritis Rheum 56:965–971. doi:10.1002/art.22416
27. 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
28. Correll CK, Binstadt BA (2014) Advances in the pathogenesis and treatment of systemic juvenile idiopathic arthritis. Pediatr Res 75:176–183. doi:10.1038/pr.2013.187
29. Arici ZS, Batu ED, Ozen S (2015) Reviewing the recommendations for lupus in children. Curr Rheumatol Rep 17:17. doi:10.1007/s11926-014-0489-5
30. Gupta A, Tyrrell P, Valani R, Benseler S, Weitzman S, Abdelhaleem M (2008) The role of the initial bone marrow aspirate in the diagnosis of hemophagocytic lymphohistiocytosis. Pediatr Blood Cancer 51:402–404. doi:10.1002/pbc.21564
31. Francois B, Trimoreau F, Vignon P, Fixe P, Praloran V, Gastinne H (1997) Thrombocytopenia in the sepsis syndrome: role of hemophagocytosis and macrophage colony-stimulating factor. Am J Med 103:114–120
32. Strauss R, Neureiter D, Westenburger B, Wehler M, Kirchner T, Hahn EG (2004) Multifactorial risk analysis of bone marrow histiocytic hyperplasia with hemophagocytosis in critically ill medical patients—a postmortem clinicopathologic analysis. Crit Care Med 32:1316–1321
33. Suster S, Hilsenbeck S, Rywlin AM (1988) Reactive histiocytic hyperplasia with hemophagocytosis in hematopoietic organs: a reevaluation of the benign hemophagocytic proliferations. Hum Pathol 19:705–712
34. Henter JI, Horne A, Arico M, Egeler RM, Filipovich AH, Imashuku S, Ladisch S, McClain K, Webb D, Winiarski J, Janka G (2007) HLH-2004: diagnostic and therapeutic guidelines for hemophagocytic lymphohistiocytosis. Pediatr Blood Cancer 48:124–131. doi:10.1002/pbc.21039
35. Parodi A, Davi S, Pringe AB, Pistorio A, Ruperto N, Magni-Manzoni S, Miettunen P, Bader-Meunier B, Espada G, Sterba G, Wright D, Magalhaes CS, Khubchandani R, Michels H, Woo P, Iglesias A, Guseinova D, Bracaglia C, Hayward K, Wouters C, Grom A, Vivarelli M, Fischer A, Breda L, Martini A, Ravelli A, Lupus Working Group of the Paediatric Rheumatology European S (2009) Macrophage activation syndrome in juvenile systemic lupus erythematosus: a multinational multicenter study of thirty-eight patients. Arthritis Rheum 60:3388–3399. doi:10.1002/art.24883
36. Kostik MM, Dubko MF, Masalova VV, Snegireva LS, Kornishina TL, Chikova IA, Likhacheva TS, Isupova EA, Glebova NI, Kuchinskaya EM, Balbotkina EV, Buchinskaya NV, Kalashnikova OV, Chasnyk VG (2015) Identification of the best cutoff points and clinical signs specific for early recognition of macrophage activation syndrome in active systemic juvenile idiopathic arthritis. Semin Arthritis Rheum 44:417–422. doi:10.1016/j.semarthrit.2014.09.004
37. Ravelli A, Minoia F, Davi S, Horne A, Bovis F, Pistorio A, Arico M, Avcin T, Behrens EM, De Benedetti F, Filipovic L, Grom AA, Henter JI, Ilowite NT, Jordan MB, Khubchandani R, Kitoh T, Lehmberg K, Lovell DJ, Miettunen P, Nichols KE, Ozen S, Pachlopnik Schmid J, Ramanan AV, Russo R, Schneider R, Sterba G, Uziel Y, Wallace C, Wouters C, Wulffraat N, Demirkaya E, Brunner HI, Martini A, Ruperto N, Cron RQ, Paediatric Rheumatology International Trials Organisation tCA, Rheumatology Research Alliance tPRCSG, The Histiocyte S (2016) 2016 Classification Criteria for Macrophage Activation Syndrome Complicating Systemic Juvenile Idiopathic Arthritis: A European League Against Rheumatism/American College of Rheumatology/Paediatric Rheumatology International Trials Organisation Collaborative Initiative. Ann Rheum Dis 75:481–489. doi:10.1136/annrheumdis-2015-208982
38. Demirkaya E, Ozen S, Bilginer Y, Ayaz NA, Makay BB, Unsal E, Erguven M, Poyrazoglu H, Kasapcopur O, Gok F, Akman S, Balat A, Cavkaytar O, Kaya B, Duzova A, Ozaltin F, Topaloglu R, Besbas N, Bakkaloglu A, Arisoy N, Ozdogan H, Bakkaloglu S, Turker T (2011) The distribution of juvenile idiopathic arthritis in the eastern Mediterranean: results from the registry of the Turkish Paediatric Rheumatology Association. Clin Exp Rheumatol 29(1):111–116
39. Ravelli A, Minoia F, Davi S, Horne A, Bovis F, Pistorio A, Arico M, Avcin T, Behrens EM, De Benedetti F, Filipovic A, Grom AA, Henter JI, Ilowite NT, Jordan MB, Khubchandani R, Kitoh T, Lehmberg K, Lovell DJ, Miettunen P, Nichols KE, Ozen S, Pachlopnik Schmid J, Ramanan AV, Russo R, Schneider R, Sterba G, Uziel Y, Wallace C, Wouters C, Wulffraat N, Demirkaya E, Brunner HI, Martini A, Ruperto N, Cron RQ (2016) Expert consensus on dynamics of laboratory tests for diagnosis of macrophage activation syndrome complicating systemic juvenile idiopathic arthritis. RMD Open 2:e000161. doi:10.1136/rmdopen-2015-000161
40. Granata G, Didona D, Stifano G, Feola A, Granata M (2015) Macrophage activation syndrome as onset of systemic lupus erythematosus: a case report and a review of the literature. Case Rep Med 2015:294041. doi:10.1155/2015/294041
41. Boom V, Anton J, Lahdenne P, Quartier P, Ravelli A, Wulffraat NM, Vastert SJ (2015) Evidence-based diagnosis and treatment of macrophage activation syndrome in systemic juvenile idiopathic arthritis. Pediatr Rheumatol Online J 13:55. doi:10.1186/s12969-015-0055-3
42. Singh S, Chandrakasan S, Ahluwalia J, Suri D, Rawat A, Ahmed N, Das R, Sachdeva MU, Varma N (2012) Macrophage activation syndrome in children with systemic onset juvenile idiopathic arthritis: clinical experience from northwest India. Rheumatol Int 32:881–886. doi:10.1007/s00296-010-1711-z
43. Cortis E, Insalaco A (2006) Macrophage activation syndrome in juvenile idiopathic arthritis. Acta Paediatr 95:38–41. doi:10.1080/08035320600649713
44. Miettunen PM, Narendran A, Jayanthan A, Behrens EM, Cron RQ (2011) Successful treatment of severe paediatric rheumatic disease-associated macrophage activation syndrome with interleukin-1 inhibition following conventional immunosuppressive therapy: case series with 12 patients. Rheumatology (Oxford) 50:417–419. doi:10.1093/rheumatology/keq218
45. Prahalad S, Bove KE, Dickens D, Lovell DJ, Grom AA (2001) Etanercept in the treatment of macrophage activation syndrome. J Rheumatol 28:2120–2124
46. Lin CI, Yu HH, Lee JH, Wang LC, Lin YT, Yang YH, Chiang BL (2012) Clinical analysis of macrophage activation syndrome in pediatric patients with autoimmune diseases. Clin Rheumatol 31:1223–1230. doi:10.1007/s10067-012-1998-0
47. De Benedetti F, Brunner HI, Ruperto N, Kenwright A, Wright S, Calvo I, Cuttica R, Ravelli A, Schneider R, Woo P, Wouters C, Xavier R, Zemel L, Baildam E, Burgos-Vargas R, Dolezalova P, Garay SM, Merino R, Joos R, Grom A, Wulffraat N, Zuber Z, Zulian F, Lovell D, Martini A, Printo Prcsg (2012) Randomized trial of tocilizumab in systemic juvenile idiopathic arthritis. N Engl J Med 367:2385–2395. doi:10.1056/NEJMoa1112802
48. Kostik MM, Dubko MF, Masalova VV, Snegireva LS, Kornishina TL, Chikova IA, Isupova EA, Kuchinskaya EM, Glebova NI, Buchinskaya NV, Kalashnikova OV, Chasnyk VG (2015) Successful treatment with tocilizumab every 4 weeks of a low disease activity group who achieve a drug-free remission in patients with systemic-onset juvenile idiopathic arthritis. Pediatr Rheumatol Online J 13:4. doi:10.1186/1546-0096-13-4
49. Ruperto N, Brunner HI, Quartier P, Constantin T, Wulffraat N, Horneff G, Brik R, McCann L, Kasapcopur O, Rutkowska-Sak L, Schneider R, Berkun Y, Calvo I, Erguven M, Goffin L, Hofer M, Kallinich T, Oliveira SK, Uziel Y, Viola S, Nistala K, Wouters C, Cimaz R, Ferrandiz MA, Flato B, Gamir ML, Kone-Paut I, Grom A, Magnusson B, Ozen S, Sztajnbok F, Lheritier K, Abrams K, Kim D, Martini A, Lovell DJ, Printo Prcsg (2012) Two randomized trials of canakinumab in systemic juvenile idiopathic arthritis. N Engl J Med 367:2396–2406. doi:10.1056/NEJMoa1205099
50. Carvalheiras G, Anjo D, Mendonca T, Vasconcelos C, Farinha F (2010) Hemophagocytic syndrome as one of the main primary manifestations in acute systemic lupus erythematosus—case report and literature review. Lupus 19:756–761. doi:10.1177/0961203309354906
51. Zeng HS, Xiong XY, Wei YD, Wang HW, Luo XP (2008) Macrophage activation syndrome in 13 children with systemic-onset juvenile idiopathic arthritis. World J Pediatr 4:97–101. doi:10.1007/s12519-008-0018-6
52. Ringold S, Weiss PF, Beukelman T, DeWitt EM, Ilowite NT, Kimura Y, Laxer RM, Lovell DJ, Nigrovic PA, Robinson AB, Vehe RK, American Collge of R (2013) 2013 update of the 2011 American College of Rheumatology recommendations for the treatment of juvenile idiopathic arthritis: recommendations for the medical therapy of children with systemic juvenile idiopathic arthritis and tuberculosis screening among children receiving biologic medications. Arthritis Rheum 65:2499–2512. doi:10.1002/art.38092