The safety of pharmacologic options for the treatment of persons with hemophilia

References

• Mannucci PM, Tuddenham EG. The hemophilias – from royal genes to gene therapy. N Engl J Med. 2001;344:1773–1779.
   PubMed Web of Science ®Google Scholar
• Berntorp E, Shapiro AD. Modern haemophilia care. Lancet. 2012;379:1447–1456.
   PubMed Web of Science ®Google Scholar
• White GC, Rosendaal F, Aledort LM, et al. Definitions in hemophilia. Recommendation of the scientific subcommittee on factor VIII and factor IX of the scientific and standardization committee of the International Society on Thrombosis and Haemostasis. Thromb Haemost. 2001;85:560.
   PubMed Web of Science ®Google Scholar
• Manco-Johnson MJ, Abshire TC, Shapiro AD, et al. Prophylaxis versus episodic treatment to prevent joint disease in boys with severe hemophilia. N Engl J Med. 2007;357:535–544.
   PubMed Web of Science ®Google Scholar
• Gringeri A, Lundin B, von Mackensen S, et al. A randomized clinical trial of prophylaxis in children with hemophilia A (the ESPRIT study). J Thromb Haemost. 2011;9:700–710.
   PubMed Web of Science ®Google Scholar
• Mannucci PM. Hemophilia: treatment options in the twenty-first century. J Thromb Haemost. 2003;1:1349–1355.
   PubMed Web of Science ®Google Scholar
• Franchini M, Mannucci PM. Past, present and future of hemophilia: a narrative review. Orphanet J Rare Dis. 2012;7:24.
   PubMed Web of Science ®Google Scholar
• Franchini M, Mannucci PM. Hemophilia A in the third millennium. Blood Rev. 2013;27:179–184.
   PubMed Web of Science ®Google Scholar
• Key NS. Inhibitors in congenital coagulation disorders. Br J Haematol. 2004;127:379–391.
   PubMed Web of Science ®Google Scholar
• Franchini M, Mannucci PM. Inhibitors of propagation of coagulation (factors VIII, IX and XI): a review of current therapeutic practice. Br J Pharmacol. 2011;72:553–562.
   Web of Science ®Google Scholar
• Giangrande P. The future of hemophilia treatment: longer-acting factor concentrates versus gene therapy. Semin Thromb Hemost. 2016;42:513–517.
   PubMed Web of Science ®Google Scholar
• Franchini M, Favaloro EJ, Lippi G. Newer hemostatic agents. Semin Thromb Hemost. 2015;41:802–808.
   PubMed Web of Science ®Google Scholar
• Fletcher ML, Trowell JM, Craske J, et al. Non-A non-B hepatitis after transfusion of factor VIII in infrequently treated patients. Br Med J. 1983;287:1754–1757.
   PubMed Web of Science ®Google Scholar
• Kernoff PBA, Lee CA, Karayiannis P, et al. High risk of non-A, non-B hepatitis after a first exposure to volunteer or commercial clotting factor concentrates: effects of prophylactic immune serum globulin. Br J Haematol. 1985;60:469–479.
   PubMed Web of Science ®Google Scholar
• Gringeri A, Mannucci PM. National survey of human immunodeficiency virus infection in Italian hemophiliacs: 1983–1987. The Medical-Scientific Committee of the Fondazione dell’Emofilia. Ric Clin Lab. 1988;18:275–280.
   PubMedGoogle Scholar
• Tabor E. The epidemiology of virus transmission by plasma derivatives: clinical studies verifying the lack of transmission of hepatitis B and C viruses and HIV type 1. Transfusion. 1999;39:1160–1168.
   PubMed Web of Science ®Google Scholar
• Centers for Disease Control and Prevention (CDC). Blood safety monitoring among persons with bleeding disorders – United States, May 1998–June 2002. MMWR Morb Mortal Wkly Rep. 2003;51:1152–1154.
   PubMedGoogle Scholar
• Makris M, Calizzani G, Fischer K, et al. EUHASS: the European Haemophilia Safety Surveillance System. Thromb Res. 2011;127 Suppl 2:S22–S25.
   PubMed Web of Science ®Google Scholar
• Farrugia A. Safety issues of plasma-derived products for treatment of inherited bleeding disorders. Semin Thromb Hemost. 2016;42:583–588
   PubMed Web of Science ®Google Scholar
• Franchini M, Lippi G. Recombinant FVIII products. Semin Thromb Hemost. 2010;36:537–549.
   PubMed Web of Science ®Google Scholar
• Azzi A, De Santis R, Morfini M, et al. TTvirus contaminates first-generation recombinant factor VIII concentrates. Blood. 2001;98:2571–2573.
   PubMed Web of Science ®Google Scholar
• Ludlam CA, Powderly WG, Bozzette S, et al. Clinical perspectives of emerging pathogens in bleeding disorders. Lancet. 2006;367:252–261.
   PubMed Web of Science ®Google Scholar
• Di Minno G, Canaro M, Ironside JW, et al. Pathogen safety of long-term treatments for bleeding disorders: (un)predictable risks and evolving threats. Semin Thromb Haemost. 2013;39:779–793.
   PubMed Web of Science ®Google Scholar
• Azzi A, Ciappi S, Zakvrzewska K, et al. Human parvovirus B 19 infection in hemophiliacs first infused with two high-purity, virally attenuated, factor VIII concentrates. Am J Hematol. 1992;39:228–230.
   PubMed Web of Science ®Google Scholar
• Soucie JM, De Staercke C, Monahan PE, et al.; US Hemophilia Treatment Center Network. Evidence for the transmission of parvovirus B19 in patients with bleeding disorders treated with plasma-derived factor concentrates in the era of nucleic acid test screening. Transfusion. 2013;53:1217–1225.
   PubMed Web of Science ®Google Scholar
• European Medicines Agency (EMEA). Press release. Supply shortages of Cerezyme and Fabrazyme – priority access for patients most in need of treatment recommended. 2009 Jun 25.
   Google Scholar
• Peden A, McCardle L, Head MW, et al. Variant CJD infection in the spleen of a neurologically asymptomatic UK adult patient with haemophilia. Haemophilia. 2010;16:296–304.
   PubMed Web of Science ®Google Scholar
• Zaman SM, Hill FG, Palmer B, et al. The risk of variant Creutzfeldt-Jakob disease among UK patients with bleeding disorders, known to have received potentially contaminated plasma products. Haemophilia. 2011;17:931–937.
   PubMed Web of Science ®Google Scholar
• Brown P, Cervenakova L, McShane LM, et al. Further studies of blood infectivity in an experimental model of transmissible spongiform encephalopathy, with an explanation of why blood components do not transmit Creutzfeldt-Jakob disease in humans. Transfusion. 1999;39:1169–1178.
   PubMed Web of Science ®Google Scholar
• Brown P. Blood infectivity, processing and screening tests in transmissible spongiform encephalopathy. Vox Sang. 2005;89:63–70.
   PubMed Web of Science ®Google Scholar
• Franchini M. Current management of hemophilia B: recommendations, complications and emerging issues. Expert Rev Hematol. 2014;7:573–581.
   PubMed Web of Science ®Google Scholar
• Astermark J. Inhibitor development: patient-determined risk factors. Haemophilia. 2010;16:66–70.
   PubMed Web of Science ®Google Scholar
• Hironaka T, Furukawa K, Esmon PC, et al. Comparative study of the sugar chains of factor VIII purified from human plasma and from the culture media of recombinant baby hamster kidney cells. J Biol Chem. 1992;267:8012–8020.
   PubMed Web of Science ®Google Scholar
• Dasgupta S, Repesse Y, Bayry J, et al. VWF protects FVIII from endocytosis by dendritic cells and subsequent presentation to immune effectors. Blood. 2007;109:610–612.
   PubMed Web of Science ®Google Scholar
• Mannucci PM, Shi Q, Bonanad S, et al. Novel investigations on the protective role of the FVIII/VWF complex in inhibitor development. Haemophilia. 2014;20 Suppl 6:2–16.
   PubMed Web of Science ®Google Scholar
• Wight J, Paisley S. The epidemiology of inhibitors in haemophilia A: a systematic review. Haemophilia. 2003;9:418–435.
   PubMed Web of Science ®Google Scholar
• Iorio A, Halimeh S, Holzhauer S, et al. Rate of inhibitor development in previously untreated hemophilia A patients treated with plasma-derived or recombinant factor VIII concentrates: a systematic review. J Thromb Haemost. 2010;8:1256–1265.
   PubMed Web of Science ®Google Scholar
• Marcucci M, Mancuso ME, Santagostino E, et al. Type and intensity of FVIII exposure on inhibitor development in PUPs with haemophilia A. A patient-level meta-analysis. Thromb Haemost. 2015;113:958–967.
   PubMed Web of Science ®Google Scholar
• Franchini M, Tagliaferri A, Mengoli C, et al. Cumulative inhibitor incidence in previously untreated patients with severe hemophilia A treated with plasma-derived versus recombinant factor VIII concentrates: a critical systematic review. Crit Rev Oncol Hematol. 2012;81:82–93.
   PubMed Web of Science ®Google Scholar
• Mancuso ME, Mannucci PM, Rocino A, et al. Source and purity of factor VIII products as risk factors for inhibitor development in patients with hemophilia A. J Thromb Haemost. 2012;10:781–790.
   PubMed Web of Science ®Google Scholar
• Gouw SC, Van Der Bom JG, Ljung R, et al. Factor VIII products and inhibitor development in severe hemophilia A. N Engl J Med. 2013;368:231–239.
   PubMed Web of Science ®Google Scholar
• Calvez T, Chambost H, Claeyssens-Donadel S, et al. Recombinant factor VIII products and inhibitor development in previously untreated boys with severe hemophilia A. Blood. 2014;124:3398–3408.
   PubMed Web of Science ®Google Scholar
• Collins PW, Palmer BP, Chalmers EA, et al. Factor VIII brand and the incidence of factor VIII inhibitors in previously untreated UK children with severe hemophilia A, 2000–2011. Blood. 2014;124:3389–3397.
   PubMed Web of Science ®Google Scholar
• Fischer K, Lassila R, Peyvandi F, et al. Inhibitor development in haemophilia according to concentrate. Four-year results from the European HAemophilia Safety Surveillance (EUHASS) project. Thromb Haemost. 2015;113:968–975.
   PubMed Web of Science ®Google Scholar
• Peyvandi F, Mannucci PM, Garagiola I, et al. Source of factor VIII replacement (plasmatic or recombinant) and incidence of inhibitory alloantibodies in previously untreated patients with severe hemophilia A: the multicenter randomized SIPPET study. N Engl J Med. 2016;374:2054–2064.
   PubMed Web of Science ®Google Scholar
• Scharrer I. The need for highly purified products to treat hemophilia B. Acta Haematologica. 1995;94 Suppl 1:2–7.
   PubMed Web of Science ®Google Scholar
• Mannucci PM, Bauer KA, Gringeri A, et al. Thrombin generation is not increased in the blood of hemophilia B patients after the infusion of a purified factor IX concentrate. Blood. 1990;76:2540–2545.
   PubMed Web of Science ®Google Scholar
• Hampton KK, Preston FE, Lowe GD, et al. Reduced coagulation activation following infusion of a highly purified factor IX concentrate compared to a prothrombin complex concentrate. Br J Haematol. 1993;84:279–284.
   PubMed Web of Science ®Google Scholar
• Coppola A, Franchini M, Makris M, et al. Thrombotic adverse events to coagulation factor concentrates for treatment of patients with haemophilia and von Willebrand disease: a systematic review of prospective studies. Haemophilia. 2012;18:e173–87.
   PubMed Web of Science ®Google Scholar
• Ehrlich HJ, Henzl MJ, Gomperts ED. Safety of factor VIII inhibitor bypass activity (FEIBA): 10-year compilation of thrombotic adverse events. Haemophilia. 2002;8:83–90.
   PubMed Web of Science ®Google Scholar
• Roberts HR, Monroe DM 3rd, Hoffman M. Safety profile of recombinant factor VIIa. Semin Hematol. 2004;41(Suppl 1):101–108.
   PubMed Web of Science ®Google Scholar
• Aledort LM. Comparative thrombotic event incidence after infusion of recombinant factor VIIa versus factor VIII inhibitor bypass activity. J Thromb Haemost. 2004;2:1700–1708.
   PubMed Web of Science ®Google Scholar
• Franchini M, Coppola A, Tagliaferri A, et al. FEIBA versus NovoSeven in hemophilia patients with inhibitors. Semin Thromb Hemost. 2013;39:772–778.
   PubMed Web of Science ®Google Scholar
• Aledort LM. Factor VIII inhibitor bypassing activity (FEIBA) – addressing safety issues. Haemophilia. 2008;14:39–43.
   PubMed Web of Science ®Google Scholar
• Franchini M, Makris M, Santagostino E, et al. Non-thrombotic-, non-inhibitor-associated adverse reactions to coagulation factor concentrates for treatment of patients with hemophilia and von Willebrand’s disease: a systematic review of prospective studies. Haemophilia. 2012;18:e164–e172.
   PubMed Web of Science ®Google Scholar
• Franchini M, Mannucci PM. The history of hemophilia. Semin Thromb Hemost. 2014;40:571–576.
   PubMed Web of Science ®Google Scholar
• Tagliaferri A, Rivolta GF, Iorio A, et al.; Italian Association of Hemophilia Centers. Mortality and causes of death in Italian persons with haemophilia, 1990-–2007. Haemophilia. 2010;16:437–446.
   PubMed Web of Science ®Google Scholar
• Mannucci PM, Mancuso ME, Franchini M. Tailoring hemostatic therapies to lower inhibitor development in previously untreated patients with severe hemophilia A. J Thromb Haemost. 2016. doi:10.1111/jth.13356. [Epub ahead of print]
   PubMed Web of Science ®Google Scholar
• Kannicht C, Ramstrom M, Kohla G, et al. Characterisation of the post-translational modifications of a novel, human cell line-derived recombinant human factor VIII. Thromb Res. 2013;131:78–88.
   PubMed Web of Science ®Google Scholar
• Mannucci PM. Half-life extension technologies for haemostatic agents. Thromb Haemost. 2015;113:165–176.
   PubMed Web of Science ®Google Scholar
• Berntorp E, Andersson NG. Prophylaxis for hemophilia in the era of extended half-life factor VIII/factor IX products. Semin Thromb Hemost. 2016;42:518–525.
   PubMed Web of Science ®Google Scholar
• Shetty S, Ghosh K. Novel therapeutic approaches for haemophilia. Haemophilia. 2015;21:152–161.
   PubMed Web of Science ®Google Scholar
• Peyvandi F, Garagiola I, Seregni S. Future of coagulation factor replacement therapy. J Thromb Haemost. 2013;11 Suppl 1:84–98.
   PubMed Web of Science ®Google Scholar
• Mannucci PM, Mancuso ME, Santagostino E, et al. Innovative pharmacological therapies for the hemophilias not based on deficient factor replacement. Semin Thromb Hemost. 2016;42:526–532.
   Google Scholar