Macrophage activation syndrome and cytokine-directed therapies

Best Practice and Research: Clinical Rheumatology

Volumn 28, Issue 2, 2014, Pages 277-292

  Schulert, Grant S ^a   Grom, Alexei A ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Hemophagocytic lymphohistiocytosis; IFN ; IL 1; IL 18; IL 6; Macrophage activation syndrome; Still's disease; Systemic juvenile idiopathic arthritis

Indexed keywords

BIOLOGICAL PRODUCT; CANAKINUMAB; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 1; INTERLEUKIN 18; INTERLEUKIN 6; RECOMBINANT INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; TOCILIZUMAB;

ARTICLE; BIOLOGICAL THERAPY; CYTOPENIA; HEMOPHAGOCYTIC SYNDROME; HUMAN; JUVENILE RHEUMATOID ARTHRITIS; MACROPHAGE ACTIVATION SYNDROME; MORBIDITY; MORTALITY; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION;

HEMOPHAGOCYTIC LYMPHOHISTIOCYTOSIS; IFNΓ; IL-1; IL-18; IL-6; MACROPHAGE ACTIVATION SYNDROME; STILL'S DISEASE; SYSTEMIC JUVENILE IDIOPATHIC ARTHRITIS;

ANIMALS; ARTHRITIS, JUVENILE; BIOLOGICAL FACTORS; CYTOKINES; DISEASE MODELS, ANIMAL; HUMANS; INTERLEUKIN-1; INTERLEUKIN-6; LYMPHOHISTIOCYTOSIS, HEMOPHAGOCYTIC; MACROPHAGE ACTIVATION SYNDROME; T-LYMPHOCYTES;

EID: 84903279667     PISSN: 15216942     EISSN: 15321770     Source Type: Journal    
DOI: 10.1016/j.berh.2014.03.002     Document Type: Review

References (120)

1. M. Hadchouel, A.M. Prieur, and C. Griscelli Acute hemorrhagic, hepatic, and neurologic manifestations in juvenile rheumatoid arthritis: possible relationship to drugs or infection Journal of Pediatrics 106 1985 561 566
2. R. Mouy, J.L. Stephan, and P. Pillet et al. Efficacy of cyclosporine A in the treatment of macrophage activation syndrome in juvenile arthritis: report of five cases Journal of Pediatrics 129 1996 750 754
3. A.A. Grom, and M. Passo Macrophage activation syndrome in systemic juvenile rheumatoid arthritis Journal of Pediatrics 129 1996 630 632
4. A. Ravelli, F. De Benedetti, S. Viola, and A. Martini Macrophage activation syndrome in systemic juvenile rheumatoid arthritis successfully treated with cyclosporine Journal of Pediatrics 128 1996 275 278
5. J.L. Stephan, I. Kone-Paut, and C. Galambrun et al. Reactive haemophagocytic syndrome in children with inflammatory disorders. A retrospective study of 24 patients Rheumatology 40 2001 1285 1292
6. S. Sawhney, P. Woo, and K.J. Murray Macrophage activation syndrome: a potentially fatal complication of rheumatic disorders Arch Dis Child 85 2001 421 426
7. B.H. Athreya Is macrophage activation syndrome a new entity? Clin Exp Rheumatol 20 2002 121 123
8. A.V. Ramanan, and R. Schneider Macrophage activation syndrome following initiation of etanercept in a child with systemic onset juvenile rheumatoid arthritis J Rheumatol 30 2003 401 403
9. B.E. Favara, A.C. Feller, and M. Pauli et al. Contemporary classification of histiocytic disorders. The WHO Committee on Histiocytic/Reticulum Cell Proliferations. Reclassification Working Group of the Histiocyte Society Med Pediatr Oncol 29 1997 157 166
10. A. Filipovich, K. McClain, and A. Grom Histiocytic disorders: recent insights into pathophysiology and practical guidelines Biol Blood Marrow Transplant 16 2010 S82 S89
11. M.B. Jordan, C.E. Allen, and S. Weitzman et al. How I treat hemophagocytic lymphohistiocytosis Blood 118 2011 4041 4052
12. K.J. Zhang, M.B. Jordan, and P. Klein et al. Hemophagocytic lymphohistiocytosis in adults Pediatr Blood Cancer 56 2011 702
13. A. Parodi, S. Davi, and A.B. Pringe et al. Macrophage activation syndrome in juvenile systemic lupus erythematosus: a multinational multicenter study of thirty-eight patients Arthritis Rheum 60 2009 3388 3399
14. T. Avcin, S.M. Tse, and R. Schneider et al. Macrophage activation syndrome as the presenting manifestation of rheumatic diseases in childhood Journal of Pediatrics 148 2006 683 686
15. G.A. Latino, C. Manlhiot, and R.S. Yeung et al. Macrophage activation syndrome in the acute phase of Kawasaki disease J Pediatr Hematol Oncol 32 2010 527 531
16. G. Simonini, I. Pagnini, and L. Innocenti et al. Macrophage activation syndrome/Hemophagocytic Lymphohistiocytosis and Kawasaki disease Pediatr Blood Cancer 55 2010 592
17. C.I. Lin, H.H. Yu, and J.H. Lee et al. Clinical analysis of macrophage activation syndrome in pediatric patients with autoimmune diseases Clin Rheumatol 31 2012 1223 1230
18. R. Dhote, J. Simon, and T. Papo et al. Reactive hemophagocytic syndrome in adult systemic disease: report of twenty-six cases and literature review Arthritis Rheum 49 2003 633 639
19. M. Atteritano, A. David, and G. Bagnato et al. Haemophagocytic syndrome in rheumatic patients. A systematic review Eur Rev Med Pharmacol Sci 16 2012 1414 1424
20. M.H. Moradinejad, and V. Ziaee The incidence of macrophage activation syndrome in children with rheumatic disorders Minerva Pediatr 63 2011 459 466
21. J. Bleesing, A. Prada, and D.M. Siegel et al. 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 2007 965 971
22. E.M. Behrens, T. Beukelman, M. Paessler, and R.Q. Cron Occult macrophage activation syndrome in patients with systemic juvenile idiopathic arthritis J Rheumatol 34 2007 1133 1138
23. J.I. Henter, A. Horne, and M. Arico et al. HLH-2004: diagnostic and therapeutic guidelines for hemophagocytic lymphohistiocytosis Pediatr Blood Cancer 48 2007 124 131
24. A. Ravelli Toward an understanding of the long-term outcome of juvenile idiopathic arthritis Clin Exp Rheumatol 22 2004 271 275
25. S. Davi, A. Consolaro, and D. Guseinova et al. An international consensus survey of diagnostic criteria for macrophage activation syndrome in systemic juvenile idiopathic arthritis J Rheumatol 38 2011 764 768
26. S.E. Stepp, R. Dufourcq-Lagelouse, and F. Le Deist et al. Perforin gene defects in familial hemophagocytic lymphohistiocytosis Science 286 1999 1957 1959
27. J. Feldmann, I. Callebaut, and G. Raposo et al. Munc13-4 is essential for cytolytic granules fusion and is mutated in a form of familial hemophagocytic lymphohistiocytosis (FHL3) Cell 115 2003 461 473
28. U. zur Stadt, S. Schmidt, and A.S. Diler et al. Linkage of familial hemophagocytic lymphohistiocytosis (FHL) type-4 to chromosome 6q24 and identification of mutations in syntaxin 11 Hum Mol Genet 14 2005 827 834
29. K. Crozat, K. Hoebe, and S. Ugolini et al. Jinx, an MCMV susceptibility phenotype caused by disruption of Unc13d: a mouse model of type 3 familial hemophagocytic lymphohistiocytosis J Exp Med 204 2007 853 863
30. U. zur Stadt, J. Rohr, and W. Seifert et al. Familial hemophagocytic lymphohistiocytosis type 5 (FHL-5) is caused by mutations in Munc18-2 and impaired binding to syntaxin 11 Am J Hum Genet 85 2009 482 492
31. S.F. Bode, K. Lehmberg, and A. Maul-Pavicic et al. Recent advances in the diagnosis and treatment of hemophagocytic lymphohistiocytosis Arthritis Res Ther 14 2012 213
32. A.A. Grom, J. Villanueva, and S. Lee et al. Natural killer cell dysfunction in patients with systemic-onset juvenile rheumatoid arthritis and macrophage activation syndrome Journal of Pediatrics 142 2003 292 296
33. M.M. Hazen, A.L. Woodward, and I. Hofmann et al. Mutations of the hemophagocytic lymphohistiocytosis-associated gene UNC13D in a patient with systemic juvenile idiopathic arthritis Arthritis Rheum 58 2008 567 570
34. K. Zhang, J. Biroschak, and D.N. Glass et al. Macrophage activation syndrome in patients with systemic juvenile idiopathic arthritis is associated with MUNC13-4 polymorphisms Arthritis Rheum 58 2008 2892 2896
35. S.J. Vastert, R. van Wijk, and L.E. D'Urbano et al. Mutations in the perforin gene can be linked to macrophage activation syndrome in patients with systemic onset juvenile idiopathic arthritis Rheumatology 49 2010 441 449
36. M.B. Jordan, D. Hildeman, J. Kappler, and P. Marrack An animal model of hemophagocytic lymphohistiocytosis (HLH): CD8+ T cells and interferon gamma are essential for the disorder Blood 104 2004 735 743
37. J. Pachlopnik Schmid, C.H. Ho, and F. Chretien et al. Neutralization of IFNgamma defeats haemophagocytosis in LCMV-infected perforin- and Rab27a-deficient mice EMBO Mol Med 1 2009 112 124
38. J. Pachlopnik Schmid, C.H. Ho, and J. Diana et al. A Griscelli syndrome type 2 murine model of hemophagocytic lymphohistiocytosis (HLH) Eur J Immunol 38 2008 3219 3225
39. P. Krebs, K. Crozat, and D. Popkin et al. Disruption of MyD88 signaling suppresses hemophagocytic lymphohistiocytosis in mice Blood 117 2011 6582 6588
40. V. Pascual, F. Allantaz, and E. Arce et al. Role of interleukin-1 (IL-1) in the pathogenesis of systemic onset juvenile idiopathic arthritis and clinical response to IL-1 blockade J Exp Med 201 2005 1479 1486
41. N. Fall, M. Barnes, and S. Thornton et al. Gene expression profiling of peripheral blood from patients with untreated new-onset systemic juvenile idiopathic arthritis reveals molecular heterogeneity that may predict macrophage activation syndrome Arthritis Rheum 56 2007 3793 3804
42. E.M. Behrens, S.W. Canna, and K. Slade et al. Repeated TLR9 stimulation results in macrophage activation syndrome-like disease in mice J Clin Invest 121 2011 2264 2277
43. J.I. Henter, G. Elinder, and O. Soder et al. Hypercytokinemia in familial hemophagocytic lymphohistiocytosis Blood 78 1991 2918 2922
44. J.I. Henter, B. Andersson, and G. Elinder et al. Elevated circulating levels of interleukin-1 receptor antagonist but not IL-1 agonists in hemophagocytic lymphohistiocytosis Med Pediatr Oncol 27 1996 21 25
45. J. Sumegi, M.G. Barnes, and S.V. Nestheide et al. Gene expression profiling of peripheral blood mononuclear cells from children with active hemophagocytic lymphohistiocytosis Blood 117 2011 e151-60
46. M. Shimizu, and A. Yachie Compensated inflammation in systemic juvenile idiopathic arthritis: role of alternatively activated macrophages Cytokine 60 2012 226 232
47. Y. Osugi, J. Hara, and S. Tagawa et al. Cytokine production regulating Th1 and Th2 cytokines in hemophagocytic lymphohistiocytosis Blood 89 1997 4100 4103
48. F.A. Verreck, T. de Boer, and D.M. Langenberg et al. Phenotypic and functional profiling of human proinflammatory type-1 and anti-inflammatory type-2 macrophages in response to microbial antigens and IFN-gamma- and CD40L-mediated costimulation J Leukoc Biol 79 2006 285 293
49. I. Kalampokis, A. Yoshizaki, and T.F. Tedder IL-10-producing regulatory B cells (B10 cells) in autoimmune disease Arthritis Res Ther 15 Suppl. 1 2013 S1
50. S. Federici, A. Martini, and M. Gattorno The central role of anti-IL-1 blockade in the treatment of monogenic and multi-factorial autoinflammatory diseases Front Immunol 4 2013 351
51. X.B. Ling, J.L. Park, and T. Carroll et al. Plasma profiles in active systemic juvenile idiopathic arthritis: biomarkers and biological implications Proteomics 10 2010 4415 4430
52. M. Gattorno, A. Piccini, and D. Lasiglie et al. The pattern of response to anti-interleukin-1 treatment distinguishes two subsets of patients with systemic-onset juvenile idiopathic arthritis Arthritis Rheum 58 2008 1505 1515
53. P.A. Nigrovic, M. Mannion, and F.H. Prince et al. Anakinra as first-line disease-modifying therapy in systemic juvenile idiopathic arthritis: report of forty-six patients from an international multicenter series Arthritis Rheum 63 2011 545 555
54. A. Zeft, R. Hollister, and B. LaFleur et al. Anakinra for systemic juvenile arthritis: the Rocky Mountain experience J Clin Rheumatol 15 2009 161 164
55. P. Quartier, F. Allantaz, and R. Cimaz et al. A multicentre, randomised, double-blind, placebo-controlled trial with the interleukin-1 receptor antagonist anakinra in patients with systemic-onset juvenile idiopathic arthritis (ANAJIS trial) Ann Rheum Dis 70 2011 747 754
56. N. Ruperto, H.I. Brunner, and P. Quartier et al. Two randomized trials of canakinumab in systemic juvenile idiopathic arthritis N Engl J Med 367 2012 2396 2406
57. A.A. Fitzgerald, S.A. Leclercq, and A. Yan et al. Rapid responses to anakinra in patients with refractory adult-onset Still's disease Arthritis Rheum 52 2005 1794 1803
58. F. de Benedetti, M. Massa, and P. Robbioni et al. Correlation of serum interleukin-6 levels with joint involvement and thrombocytosis in systemic juvenile rheumatoid arthritis Arthritis Rheum 34 1991 1158 1163
59. D. Lasiglie, E. Traggiai, and S. Federici et al. Role of IL-1 beta in the development of human T(H)17 cells: lesson from NLPR3 mutated patients PLoS One 6 2011 e20014
60. A.D. Billiau, T. Roskams, and R. Van Damme-Lombaerts et al. Macrophage activation syndrome: characteristic findings on liver biopsy illustrating the key role of activated, IFN-gamma-producing lymphocytes and IL-6- and TNF-alpha-producing macrophages Blood 105 2005 1648 1651
61. X.J. Xu, Y.M. Tang, and H. Song et al. Diagnostic accuracy of a specific cytokine pattern in hemophagocytic lymphohistiocytosis in children Journal of Pediatrics 160 2012 984 990 e1
62. R. Strippoli, F. Carvello, and R. Scianaro et al. 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 2012 1680 1688
63. F. De Benedetti, H.I. Brunner, and N. Ruperto et al. Randomized trial of tocilizumab in systemic juvenile idiopathic arthritis N Engl J Med 367 2012 2385 2395
64. M. Shimizu, Y. Nakagishi, and K. Kasai et al. Tocilizumab masks the clinical symptoms of systemic juvenile idiopathic arthritis-associated macrophage activation syndrome: the diagnostic significance of interleukin-18 and interleukin-6 Cytokine 58 2012 287 294
65. S. Shenoi, and C.A. Wallace Tumor necrosis factor inhibitors in the management of juvenile idiopathic arthritis: an evidence-based review Paediatr Drugs 12 2010 367 377
66. J.G. Harris, E.A. Kessler, and J.W. Verbsky Update on the treatment of juvenile idiopathic arthritis Curr Allergy Asthma Rep 13 2013 337 346
67. M. Shimizu, T. Yokoyama, and K. Yamada et al. Distinct cytokine profiles of systemic-onset juvenile idiopathic arthritis-associated macrophage activation syndrome with particular emphasis on the role of interleukin-18 in its pathogenesis Rheumatology (Oxford) 49 2010 1645 1653
68. C.K. Correll, and B.A. Binstadt Advances in the pathogenesis and treatment of systemic juvenile idiopathic arthritis Pediatr Res 75 2014 176 183
69. E.M. DeWitt, Y. Kimura, and T. Beukelman et al. Consensus treatment plans for new-onset systemic juvenile idiopathic arthritis Arthritis Care Res (Hoboken) 64 2012 1001 1010
70. L. Chiossone, S. Audonnet, and B. Chetaille et al. Protection from inflammatory organ damage in a murine model of hemophagocytic lymphohistiocytosis using treatment with IL-18 binding protein Front Immunol 3 2012 239
71. S.L. van Dommelen, N. Sumaria, and R.D. Schreiber et al. Perforin and granzymes have distinct roles in defensive immunity and immunopathology Immunity 25 2006 835 848
72. J. Maruyama, and S. Inokuma Cytokine profiles of macrophage activation syndrome associated with rheumatic diseases J Rheumatol 37 2010 967 973
73. B. Makay, S. Yilmaz, and Z. Turkyilmaz et al. Etanercept for therapy-resistant macrophage activation syndrome Ann Rheum Dis 65 2006 443
74. S. Prahalad, K.E. Bove, and D. Dickens et al. Etanercept in the treatment of macrophage activation syndrome J Rheumatol 28 2001 2120 2124
75. D. Aeberli, S. Oertle, and H. Mauron et al. Inhibition of the TNF-pathway: use of infliximab and etanercept as remission-inducing agents in cases of therapy-resistant chronic inflammatory disorders Swiss Med Wkly 132 2002 414 422
76. A. Stern, R. Riley, and L. Buckley Worsening of macrophage activation syndrome in a patient with adult onset Still's disease after initiation of etanercept therapy J Clin Rheumatol 7 2001 252 256
77. A.J. Puren, G. Fantuzzi, and C.A. Dinarello Gene expression, synthesis, and secretion of interleukin 18 and interleukin 1 beta are differentially regulated in human blood mononuclear cells and mouse spleen cells Proc Natl Acad Sci U S A 96 1999 2256 2261
78. C.A. Dinarello Interleukin-18 and the pathogenesis of inflammatory diseases Semin Nephrol 27 2007 98 114
79. O. Ludwiczek, A. Kaser, and D. Novick et al. Plasma levels of interleukin-18 and interleukin-18 binding protein are elevated in patients with chronic liver disease J Clin Immunol 22 2002 331 337
80. K. Mazodier, V. Marin, and D. Novick et al. Severe imbalance of IL-18/IL-18BP in patients with secondary hemophagocytic syndrome Blood 106 2005 3483 3489
81. N. Maeno, S. Takei, and H. Imanaka et al. Increased interleukin-18 expression in bone marrow of a patient with systemic juvenile idiopathic arthritis and unrecognized macrophage-activation syndrome Arthritis Rheum 50 2004 1935 1938
82. M. Kawashima, M. Yamamura, and M. Taniai et al. Levels of interleukin-18 and its binding inhibitors in the blood circulation of patients with adult-onset Still's disease Arthritis Rheum 44 2001 550 560
83. D. Novick, B. Schwartsburd, and R. Pinkus et al. A novel IL-18BP ELISA shows elevated serum IL-18BP in sepsis and extensive decrease of free IL-18 Cytokine 14 2001 334 342
84. D. Novick, D. Elbirt, and G. Miller et al. High circulating levels of free interleulkin-18 in patients with active SLE in the presence of elevated levels of interleukin-18 binding protein Cytokine 48 2009 103 104
85. F. Favilli, C. Anzilotti, and L. Martinelli et al. IL-18 activity in systemic lupus erythematosus Ann N Y Acad Sci 1173 2009 301 309
86. D. Novick, D. Elbirt, and C.A. Dinarello et al. Interleukin-18 binding protein in the Sera of patients with Wegener's granulomatosis J Clin Immunol 29 2009 38 45
87. W. de Jager, S.J. Vastert, and J.M. Beekman et al. Defective phosphorylation of interleukin-18 receptor beta causes impaired natural killer cell function in systemic-onset juvenile idiopathic arthritis Arthritis Rheum 60 2009 2782 2793
88. H. Kampfer, J. Paulukat, and H. Muhl et al. Lack of interferon-gamma production despite the presence of interleukin-18 during cutaneous wound healing Mol Med 6 2000 1016 1027
89. C.A. Nold-Petry, T. Lehrnbecher, and A. Jarisch et al. Failure of interferon gamma to induce the anti-inflammatory interleukin 18 binding protein in familial hemophagocytosis Plos One 5 2010
90. K. Schroder, P.J. Hertzog, T. Ravasi, and D.A. Hume Interferon-gamma: an overview of signals, mechanisms and functions J Leukoc Biol 75 2004 163 189
91. D.M. Mosser The many faces of macrophage activation J Leukoc Biol 73 2003 209 212
92. A. Mantovani, A. Sica, and S. Sozzani et al. The chemokine system in diverse forms of macrophage activation and polarization Trends Immunol 25 2004 677 686
93. E.E. Zoller, J.E. Lykens, and C.E. Terrell et al. Hemophagocytosis causes a consumptive anemia of inflammation J Exp Med 208 2011 1203 1214
94. F.O. Martinez, A. Sica, A. Mantovani, and M. Locati Macrophage activation and polarization Front Biosci 13 2008 453 461
95. K.A. Sikora, N. Fall, S. Thornton, and A.A. Grom The limited role of interferon-gamma in systemic juvenile idiopathic arthritis cannot be explained by cellular hyporesponsiveness Arthritis Rheum 64 2012 3799 3808
96. E.M. Ogilvie, A. Khan, and M. Hubank et al. Specific gene expression profiles in systemic juvenile idiopathic arthritis Arthritis Rheum 56 2007 1954 1965
97. X. Hu, and L.B. Ivashkiv Cross-regulation of signaling pathways by interferon-gamma: implications for immune responses and autoimmune diseases Immunity 31 2009 539 550
98. H. Takada, Y. Takahata, and A. Nomura et al. Increased serum levels of interferon-gamma-inducible protein 10 and monokine induced by gamma interferon in patients with haemophagocytic lymphohistiocytosis Clin Exp Immunol 133 2003 448 453
99. M. Nagasawa, Z. Yi, and S. Imashuku et al. Soluble TWEAK is markedly elevated in hemophagocytic lymphohistiocytosis Am J Hematol 83 2008 222 225
100. G. de Saint Basile, G. Menasche, and S. Latour Inherited defects causing hemophagocytic lymphohistiocytic syndrome Ann N Y Acad Sci 1246 2011 64 76
101. A. Ravelli, A.A. Grom, E.M. Behrens, and R.Q. Cron Macrophage activation syndrome as part of systemic juvenile idiopathic arthritis: diagnosis, genetics, pathophysiology and treatment Genes Immun 13 2012 289 298
102. T. Imagawa, H. Umebayashi, and R. Kurosawa et al. Differences between systemic-onset juvenile idiopathic arthritis and macrophage activation syndrome from the standpoint of the proinflammatory cytokine profile Arthritis Rheum 50 2004 S92-S
103. M.F. Ibarra, M. Klein-Gitelman, and E. Morgan et al. Serum neopterin levels as a diagnostic marker of hemophagocytic lymphohistiocytosis syndrome Clin Vaccin Immunol 18 2011 609 614
104. B. Quesnel, B. Catteau, and V. Aznar et al. Successful treatment of juvenile rheumatoid arthritis associated haemophagocytic syndrome by cyclosporin A with transient exacerbation by conventional-dose G-CSF Br J Haematol 97 1997 508 510
105. A.A. Gupta, P. Tyrrell, and R. Valani et al. Experience with hemophagocytic lymphohistiocytosis/macrophage activation syndrome at a single institution J Pediatr Hematol Oncol 31 2009 81 84
106. L. Sung, S.M. King, and M. Carcao et al. Adverse outcomes in primary hemophagocytic lymphohistiocytosis J Pediatr Hematol Oncol 24 2002 550 554
107. A. Coca, K.W. Bundy, and B. Marston et al. Macrophage activation syndrome: serological markers and treatment with anti-thymocyte globulin Clin Immunol 132 2009 10 18
108. N. Mahlaoui, M. Ouachee-Chardin, and G. de Saint Basile et al. Immunotherapy of familial hemophagocytic lymphohistiocytosis with antithymocyte globulins: a single-center retrospective report of 38 patients Pediatrics 120 2007 e622-8
109. I.J. Su, C.H. Wang, A.L. Cheng, and R.L. Chen Hemophagocytic syndrome in Epstein-Barr virus-associated T-lymphoproliferative disorders: disease spectrum, pathogenesis, and management Leuk Lymphoma 19 1995 401 406
110. C. Larroche, L. Mouthon, and N. Casadevall et al. Successful treatment of thymoma-associated pure red cell aplasia with intravenous immunoglobulins Med Pediatr Oncol 65 2000 74 76
111. A.G. Tristano, L. Casanova-Escalona, A. Torres, and M.A. Rodriguez Macrophage activation syndrome in a patient with systemic onset rheumatoid arthritis - rescue with intravenous immunoglobulin therapy JCR J Clin Rheumatol 9 2003 253 258
112. N.J. Balamuth, K.E. Nichols, M. Paessler, and D.T. Teachey Use of rituximab in conjunction with immunosuppressive chemotherapy as a novel therapy for Epstein Barr virus-associated hemophagocytic lymphohistiocytosis J Pediatr Hematol Oncol 29 2007 569 573
113. G. Bosman, S.M. Langemeijer, and K.M. Hebeda et al. The role of rituximab in a case of EBV-related lymphoproliferative disease presenting with haemophagocytosis Neth J Med 67 2009 364 365
114. A. Kelly, and A.V. Ramanan A case of macrophage activation syndrome successfully treated with anakinra Nat Clin Pract Rheumatol 4 2008 615 620
115. P.M. Miettunen, A. Narendran, and A. Jayanthan et al. 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 2011 417 419
116. N. Bruck, M. Suttorp, and M. Kabus et al. Rapid and sustained remission of systemic juvenile idiopathic arthritis-associated macrophage activation syndrome through treatment with anakinra and corticosteroids J Clin Rheumatol 17 2011 23 27
117. M. Durand, Y. Troyanov, P. Laflamme, and G. Gregoire Macrophage activation syndrome treated with anakinra J Rheumatol 37 2010 879 880
118. S. Yokota, T. Imagawa, and M. Mori et al. Efficacy and safety of tocilizumab in patients with systemic-onset juvenile idiopathic arthritis: a randomised, double-blind, placebo-controlled, withdrawal phase III trial Lancet 371 2008 998 1006
119. M. Kobayashi, Y. Takahashi, and H. Yamashita et al. Benefit and a possible risk of tocilizumab therapy for adult-onset Still's disease accompanied by macrophage-activation syndrome Mod Rheumatol 21 2011 92 96
120. E.A. Kessler, S.S. Vora, and J.W. Verbsky Risk of significant cytopenias after treatment with tocilizumab in systemic juvenile arthritis patients with a history of macrophage activation syndrome Pediatr Rheumatol Online J 10 2012 30