Emapalumab for adult and pediatric patients with hemophagocytic lymphohistiocytosis

References

• Emile JF, Abla O, Fraitag S, et al. Revised classification of histiocytoses and neoplasms of the macrophage-dendritic cell lineages. Blood. 2016 Jun 2 127;(22)2672–2681.
   PubMed Web of Science ®Google Scholar
• Marsh RA, Haddad E. How i treat primary haemophagocytic lymphohistiocytosis. Br J Haematol. 2018 Jul;182(2):185–199.
   PubMed Web of Science ®Google Scholar
• Voskoboinik I, Dunstone MA, Baran K, et al. Perforin: structure, function, and role in human immunopathology. Immunol Rev. 2010 May;235(1):35–54. .
   PubMedGoogle Scholar
• Miao Y, Zhu HY, Qiao C, et al. Pathogenic gene mutations or variants identified by targeted gene sequencing in adults with hemophagocytic lymphohistiocytosis. Front Immunol. 2019 Mar;7(10):395. .
   Google Scholar
• Jordan MB, Allen CE, Greenberg J, et al. Challenges in the diagnosis of hemophagocytic lymphohistiocytosis: recommendations from the North American Consortium for Histiocytosis (NACHO). Pediatr Blood Cancer. 2019 Nov;66(11):e27929. .
   PubMed Web of Science ®Google Scholar
• George MR. Hemophagocytic lymphohistiocytosis: review of etiologies and management. J Blood Med. 2014 Jun;12(5):69–86.
   Google Scholar
• Henter JI, Elinder G, Soder O, et al. Incidence in Sweden and clinical features of familial hemophagocytic lymphohistiocytosis. Acta Paediatr Scand. 1991 Apr;80(4):428–435.
   PubMed Web of Science ®Google Scholar
• Niece JA, Rogers ZR, Ahmad N, et al. Hemophagocytic lymphohistiocytosis in Texas: observations on ethnicity and race. Pediatr Blood Cancer. 2010 Mar;54(3):424–428. .
   PubMed Web of Science ®Google Scholar
• Janka GE. Familial hemophagocytic lymphohistiocytosis. Eur J Pediatr. 1983 Jun-Jul;140(3):221–230.
   PubMed Web of Science ®Google Scholar
• Aricò M, Janka G, Fischer A, et al. Hemophagocytic lymphohistiocytosis. report of 122 children from the International Registry. FHL Study Group of the Histiocyte Society. Leukemia. 1996 Feb;10(2):197–203.
   PubMed Web of Science ®Google Scholar
• Trottestam H, Horne AC, Aricò M, et al. Chemoimmunotherapy for hemophagocytic lymphohistiocytosis: long-term results of the HLH-94 treatment protocol. Blood. 2011 Oct 27 118;(17)4577–4584.
   PubMed Web of Science ®Google Scholar
• Henter JI, Arico M, Egeler RM, et al. HLH-94: a treatment protocol for hemophagocytic lymphohistiocytosis. HLH study Group of the Histiocyte Society. Med Pediatr Oncol. 1997 May 28;(5)342–347.
   PubMedGoogle Scholar
• Bergsten E, Horne AC, Aricó M, et al. Confirmed efficacy of etoposide and dexamethasone in HLH treatment: long-Term results of the cooperative HLH-2004 study. Blood. 2017 Dec 21 130;(25)2728–2738.
   PubMed Web of Science ®Google Scholar
• Henter JI, Horne AC, Aricó M, et al. HLH-2004: diagnostic and therapeutic guidelines for hemophagocytic lymphohistiocytosis. Pediatr Blood Cancer. 2007 Feb 48;(2)124–131.
   PubMed Web of Science ®Google Scholar
• Mahlaoui N, Ouachée-Chardin M, De Saint Basile G, et al. Immunotherapy of familial hemophagocytic lymphohistiocytosis with antithymocyte globulins: a single-center retrospective report of 38 patients. Pediatrics. 2007 Sep 120;(3)e622–8.
   PubMed Web of Science ®Google Scholar
• McClain KL. Treatment of hemophagocytic lymphohistiocytosis in the era of new biologics. Pediatr Blood Cancer. 2020 Oct;67(10):e28631.
   PubMed Web of Science ®Google Scholar
• Henter JI, Elinder G, Soder O, et al. Hypercytokinemia in familial hemophagocytic lymphohistiocytosis. Blood. 1991;78(11):2918–2922. .
   PubMed Web of Science ®Google Scholar
• Put K, Avau A, Brisse E, et al. Cytokines in systemic juvenile idiopathic arthritis and haemophagocytic lymphohistiocytosis: tipping the balance between interleukin-18 and interferon-γ. Rheumatology (Oxford). 2015 Aug 54;(8)1507–1517.
   PubMed Web of Science ®Google Scholar
• Tang Y, Xu X, Song H, et al. Early diagnostic and prognostic significance of a specific Th1/Th2 cytokine pattern in children with haemophagocytic syndrome. Br J Haematol. 2008 Oct 143;(1)84–91.
   PubMed Web of Science ®Google Scholar
• Xu XJ, Tang YM, Song H, et al. Diagnostic accuracy of a specific cytokine pattern in hemophagocytic lymphohistiocytosis in children. J Pediatr. 2012 Jun;160(6):984–990. e1.
   PubMed Web of Science ®Google Scholar
• Bracaglia C, De Graaf K, Pires Marafon D, et al. Elevated circulating levels of interferon-γ and interferon-γ-induced chemokines characterize patients with macrophage activation syndrome complicating systemic juvenile idiopathic arthritis. Ann Rheum Dis. 2017;76(1):166–172. .
   PubMed Web of Science ®Google Scholar
• Jordan MB, Hildeman D, Kappler J, et al. An animal model of hemophagocytic lymphohistiocytosis (HLH): CD8+ T cells and interferon gamma are essential for the disorder. Blood. 2004 Aug 1; 104(3):735–743.
   PubMed Web of Science ®Google Scholar
• Behrens EM, Canna SW, Slade K, et al. Repeated TLR9 stimulation results in macrophage activation syndrome-like disease in mice. J Clin Invest. 2011 Jun 121;(6)2264–2277.
   PubMed Web of Science ®Google Scholar
• Pachlopnik Schmid J, Ho CH, Chrétien F, et al. Neutralization of IFNgamma defeats haemophagocytosis in LCMV-infected perforin- and Rab27a-deficient mice. EMBO Mol Med. 2009 May 1;(2)112–124.
   PubMed Web of Science ®Google Scholar
• Kögl T, Müller J, Jessen B, et al. Hemophagocytic lymphohistiocytosis in syntaxin-11-deficient mice: t-cell exhaustion limits fatal disease. Blood. 2013 Jan 24 121;(4)604–613.
   PubMed Web of Science ®Google Scholar
• Gather R, Aichele P, Goos N, et al. Trigger‐dependent differences determine therapeutic outcome in murine primary hemophagocytic lymphohistiocytosis. Eur J Immunol. 2020 Nov 2 50;(11)1770–1782.
   PubMed Web of Science ®Google Scholar
• Brisse E, Imbrechts M, Put K, et al. Mouse cytomegalovirus infection in balb/c mice resembles virus-associated secondary hemophagocytic lymphohistiocytosis and shows a pathogenesis distinct from primary hemophagocytic lymphohistiocytosis. J Immunol. 2016 Apr 1 196;(7)3124–3134.
   PubMed Web of Science ®Google Scholar
• Humblet-Baron S, Franckaert D, Dooley J, et al. IFN-γ and CD25 drive distinct pathologic features during hemophagocytic lymphohistiocytosis. J Allergy Clin Immunol. 2019 [Jun 1];143(6):2215–2226.e7. .
   PubMed Web of Science ®Google Scholar
• Burn TN, Weaver L, Rood JE, et al. Genetic deficiency of interferon-γ reveals interferon-γ–independent manifestations of murine hemophagocytic lymphohistiocytosis. Arthritis Rheumatol. 2020 Feb;72(2):335–347. .
   PubMed Web of Science ®Google Scholar
• Merli P, Quintarelli C, Strocchio L, et al. The role of interferon-gamma and its signaling pathway in pediatric hematological disorders. Pediatr Blood Cancer. 2021 Apr;68(4):e28900.
   PubMed Web of Science ®Google Scholar
• Hatterer E, Richard F, Malinge P, et al. P156 Investigating the novel mechanism of action for NI-0501, a human interferon gamma monoclonal antibody. Cytokine. 2012 Sep 1 59;(3)570.
   Web of Science ®Google Scholar
• Locatelli F, Jordan MB, Allen C, et al. Emapalumab in children with primary hemophagocytic lymphohistiocytosis. N Engl J Med. 2020 May 7;382(19):1811–1822. .
   PubMed Web of Science ®Google Scholar
• Novimmune SA. GAMIFANTTM (emapalumab-Izsg): prescribing information. 2018.[Internet]. cited 2020 Nov 11]. Available from. : https://www.accessdata.fda.gov/drugsatfda_docs/label/2018/761107lbl.pdf.
   Google Scholar
• Al-Salama ZT. Emapalumab: first global approval. Drugs. 2019 Jan;79(1):99–103.
   PubMed Web of Science ®Google Scholar
• Benedetti FD, Brogan P, Grom A, et al. OP0204 EMAPALUMAB, AN INTERFERON GAMMA (IFN-Y)-BLOCKING MONOCLONAL ANTIBODY, IN PATIENTS WITH MACROPHAGE ACTIVATION SYNDROME (MAS) COMPLICATING SYSTEMIC JUVENILE IDIOPATHIC ARTHRITIS (SJIA). Ann Rheum Dis. 2019;78:178.
   Web of Science ®Google Scholar
• Gloude NJ, Dandoy CE, Davies SM, et al. Thinking beyond HLH: clinical features of patients with concurrent presentation of hemophagocytic lymphohistiocytosis and thrombotic microangiopathy. J Clin Immunol. 2020 Jul;40(5):699–707. .
   PubMed Web of Science ®Google Scholar
• Lounder DT, Bin Q, De Min C, et al. Treatment of refractory hemophagocytic lymphohistiocytosis with emapalumab despite severe concurrent infections. Blood Adv. 2019 Jan 8; 3(1):47–50.
   PubMed Web of Science ®Google Scholar
• Tucci F, Gallo V, Barzaghi F, et al. Treatment with emapalumab in an ADA-SCID patient with refractory hemophagocytic lymphohistiocytosis-related graft failure and disseminated BCGitis. Haematologica. 2020 Aug;13:2020.255620. haematol.
   Google Scholar
• Merli P, Caruana I, De Vito R, et al. Role of interferon-γ in immune-mediated graft failure after allogeneic hematopoietic stem cell transplantation. Haematologica. 2019 Nov;104(11):2314–2323. .
   PubMed Web of Science ®Google Scholar
• Chinello M, Balter R, De Bortoli M, et al. Chronic graft-versus-host-disease-related polymyositis: a 17-months-old child with a rare and late complication of haematopoietic stem cell transplantation. Mediterr J Hematol Infect Dis. 2020 Jan 1 12;(1)e2020002.
   PubMedGoogle Scholar
• Gabr JB, Liu E, Mian S, et al. Successful treatment of secondary macrophage activation syndrome with emapalumab in a patient with newly diagnosed adult-onset still’s disease: case report and review of the literature. Ann Transl Med. 2020 Jul;8(14):887. .
   PubMed Web of Science ®Google Scholar
• Lam MT, Coppola S, Krumbach OHF, et al. A novel disorder involving dyshematopoiesis, inflammation, and HLH due to aberrant CDC42 function. J Exp Med. 2019 Dec 2 216;(12)2778–2799.
   PubMed Web of Science ®Google Scholar
• Das R, Guan P, Sprague L, et al. Janus kinase inhibition lessens inflammation and ameliorates disease in murine models of hemophagocytic lymphohistiocytosis. Blood. 2016 Mar 31 127;(13)1666–1675.
   PubMed Web of Science ®Google Scholar
• Ahmed A, Merrill SA, Alsawah F, et al. Ruxolitinib in adult patients with secondary haemophagocytic lymphohistiocytosis: an open-label, single-centre, pilot trial. Lancet Haematol. 2019 Dec 1 6;(12)e630–7.
   PubMed Web of Science ®Google Scholar
• Zhang Q, Wei A, Ma HH, et al. A pilot study of ruxolitinib as a front-line therapy for 12 children with secondary hemophagocytic lymphohistiocytosis. Haematologica. 2020 Jul; 30: haematol 2020.253781
   Google Scholar
• Wei A, Ma H, Li Z, et al. Short-term effectiveness of ruxolitinib in the treatment of recurrent or refractory hemophagocytic lymphohistiocytosis in children. Int J Hematol. 2020 Oct;112(4):568–576. .
   PubMed Web of Science ®Google Scholar
• Trantham T, Auten J, Muluneh B, et al. Ruxolitinib for the treatment of lymphoma-associated hemophagocytic lymphohistiocytosis: a cautionary tale. J Oncol Pharm Pract. 2020 Jun;26(4):1005–1008.
   PubMed Web of Science ®Google Scholar
• Ramanan KM, Uppuluri R, Ravichandran N, et al. Successful remission induction in refractory familial hemophagocytic lymphohistiocytosis with ruxolitinib as a bridge to hematopoietic stem cell transplantation. Pediatr Blood Cancer. 2020 Mar;67(3):e28071. .
   PubMed Web of Science ®Google Scholar
• Marsh RA, Allen CE, McClain KL, et al. Salvage therapy of refractory hemophagocytic lymphohistiocytosis with alemtuzumab. Pediatr Blood Cancer. 2013 Jan;60(1):101–109. .
   PubMed Web of Science ®Google Scholar
• Ravelli A, Grom AA, Behrens EM, et al. Macrophage activation syndrome as part of systemic juvenile idiopathic arthritis: diagnosis, genetics, pathophysiology and treatment. Genes Immun. 2012 Jun;13(4):289–298.
   PubMed Web of Science ®Google Scholar
• Miettunen PM, Narendran A, Jayanthan A, 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). 2011 Feb 50;(2)417–419.
   PubMed Web of Science ®Google Scholar
• Rajasekaran S, Kruse K, Kovey K, et al. Therapeutic role of anakinra, an interleukin-1 receptor antagonist, in the management of secondary hemophagocytic lymphohistiocytosis/sepsis/multiple organ dysfunction/macrophage activating syndrome in critically ill children. Pediatr Crit Care Med. 2014 Jun 15;(5)401–408.
   PubMed Web of Science ®Google Scholar
• Eloseily EM, Weiser P, Crayne CB, et al. Benefit of anakinra in treating pediatric secondary hemophagocytic lymphohistiocytosis. Arthritis Rheumatol. 2020 Feb;72(2):326–334. .
   PubMed Web of Science ®Google Scholar
• Fitzgerald JC, Weiss SL, Maude SL, et al. Cytokine release syndrome after chimeric antigen receptor T cell therapy for acute lymphoblastic leukemia. Crit Care Med. 2017 Feb;45(2):e124–e131. .
   PubMed Web of Science ®Google Scholar
• Dufranc E, Del Bello A, Belliere J, et al. TAIDI (Toulouse Acquired Immune Deficiency and Infection) study group. IL6-R blocking with tocilizumab in critically ill patients with hemophagocytic syndrome. Crit Care. 2020 Apr 22 24;(1)166.
   PubMed Web of Science ®Google Scholar
• Bergsten E, Horne A, Hed Myrberg I, et al. Stem cell transplantation for children with hemophagocytic lymphohistiocytosis: results from the HLH-2004 study. Blood Adv. 2020 Aug 11 4;(15)3754–3766.
   PubMed Web of Science ®Google Scholar
• Allen CE, Marsh R, Dawson P, et al. Reduced-intensity conditioning for hematopoietic cell transplant for HLH and primary immune deficiencies. Blood. 2018 Sep 27 132;(13)1438–1451.
   PubMed Web of Science ®Google Scholar
• Messina C, Zecca M, Fagioli F, et al. Outcomes of children with hemophagocytic lymphohistiocytosis given allogeneic hematopoietic stem cell transplantation in italy. Biol Blood Marrow Transplant. 2018 Jun;24(6):1223–1231. .
   PubMed Web of Science ®Google Scholar