Open Access

The inhibitors – a challenge for the management of patients with hereditary haemophilia A


Cite

1. TABRINZIA-TABRIZI S., GHOLAMPOUR M., MANSOURITORGHABEH H. A close insight to factor VIII inhibitor in the congenital hemophilia A. Expert Rev Hematol. 2016; 9:903-913.10.1080/17474086.2016.120855427367203Search in Google Scholar

2. RODRIGUEZ-MERCHÁN E.C. Orthopedic surgery is possible in hemophilic patients with inhibitors. Am J Orthop (Belle Mead NJ). 2012; 41:570-574.Search in Google Scholar

3. FINN J.D., OZELO M.C., SABATINO D.E., FRANCK H.W., MERRICKS E.P., CRUDELE J.M., et al. Eradication of neutralizing antibodies to factor VIII in canine hemophilia A after liver gene therapy. Blood. 2010; 116:5842-5848.10.1182/blood-2010-06-288001303138020876851Search in Google Scholar

4. LAI J., HOUGH C., TARRANT J., LILLICRAP D. Biological considerations of plasma-derived and recombinant factor VIII immunogenicity. Blood. 2017; 129:3147-3154.10.1182/blood-2016-11-75088528432221Search in Google Scholar

5. OWAIDAH T., MOMEN A.A., ALZAHRANI H., ALMUSA A., ALKASIM F., TARAWAH A., et al. The prevalence of factor VIII and IX inhibitors among Saudi patients with hemophilia: Results from the Saudi national hemophilia screening program. Medicine (Baltimore). 2017; 96:e5456.10.1097/MD.0000000000005456526615028079788Search in Google Scholar

6. BENSON G., AUERSWALD G., ELEZOVIĆ I., LAMBERT T., LJUNG R., MORFINI M., et al. Immune tolerance induction in patients with severe hemophilia with inhibitors: expert panel views and recommendations for clinical practice. Eur J Haematol. 2012; 88:371-379.10.1111/j.1600-0609.2012.01754.x22260405Search in Google Scholar

7. ROCINO A., FRANCHINI M., COPPOLA A. Treatment and Prevention of Bleeds in Haemophilia Patients with Inhibitors to Factor VIII/IX. J Clin Med. 2017; 6;pii:E46.10.3390/jcm6040046540677828420167Search in Google Scholar

8. ECKHARDT C.L., LOOMANS J.I., VAN VELZEN A.S., PETERS M., MAUSER-BUNSHOTEN E.P., SCHWAAB R., et al. Inhibitor development and mortality in non-severe hemophilia A. J Thromb Haemost. 2015; 13:1217-1225.10.1111/jth.1299025912309Search in Google Scholar

9. FRANCHINI M., LIPPI G. Prevention of inhibitor development in hemophilia A in 2016. A glimpse into the future? Thromb Res. 2016; 148:96-100.10.1016/j.thromres.2016.10.024Search in Google Scholar

10. VAN DEN BERG H.M., HASHEMI S.M., FISCHER K., PETRINI P., LJUNG R., RAFOWICZ A., et al. Increased inhibitor incidence in severe haemophilia A since 1990 attributable to more low titre inhibitors. Thromb Haemost. 2016; 115:729-737.10.1160/TH15-08-069226632988Search in Google Scholar

11. VAN DEN BERG H.M., LJUNG R.; PEDNET STUDY GROUP. Can a “center effect” explain the higher frequency of inhibitors for a second-generation recombinant factor VIII product? Blood. 2015; 126:2164-2165.10.1182/blood-2015-08-663583Search in Google Scholar

12. FISCHER K., IORIO A., LASSILA R., PEYVANDI F., CALIZZANI G., GATT A., et al. Inhibitor development in non-severe haemophilia across Europe. Thromb Haemost. 2015; 114:670-675.10.1160/TH14-12-104426293381Search in Google Scholar

13. KARAMAN K, AKBAYRAM S, GARIPARDIÇ M, ÖNER AF. Diagnostic evaluation of our patients with hemophilia A: 17-year experience. Turk Pediatri Ars. 2015; 50:96-101.10.5152/tpa.2015.2516452399226265893Search in Google Scholar

14. BLATNY J., KOMRSKA V., BLAZEK B., PENKA M., OVESNA P.; CZECH NATIONAL HAEMOPHILIA PROGRAMME. Inhibitors incidence rate in Czech previously untreated patients with haemophilia A has not increased since introduction of recombinant factor VIII treatment in 2003. Blood Coagul Fibrinolysis. 2015; 26:673-678.10.1097/MBC.000000000000029825886834Search in Google Scholar

15. HALIMEH S., BIDLINGMAIER C., HELLER C., GUTSCHE S., HOLZHAUER S., KENET G., et al. Risk factors for high-titer inhibitor development in children with hemophilia A: results of a cohort study. Biomed Res Int. 2013; 2013:901975.10.1155/2013/901975380755924199202Search in Google Scholar

16. TUNSTALL O., ASTERMARK J. Strategies for reducing inhibitor formation in severe haemophilia. Eur J Haematol. 2015; 94 Suppl 77:45-50.10.1111/ejh.1250125560794Search in Google Scholar

17. ÁLVAREZ T., SOTO I., ASTERMARK J. Non-genetic risk factors and their influence on the management of patients in the clinic. Eur J Haematol. 2015; 94 Suppl 77:2-6.10.1111/ejh.1249425560787Search in Google Scholar

18. CARACO M., RE W., EWENSTEIN B. The role of previously untreated patient studies in understanding the development of FVIII inhibitors. Haemophilia. 2016; 22:22-31.10.1111/hae.1279026315604Search in Google Scholar

19. TER AVEST P.C., FISCHER K., MANCUSO M.E., SANTAGOSTINO E., YUSTE V.J., VAN DEN BERG H.M., et al. Risk stratification for inhibitor development at first treatment for severe hemophilia A: a tool for clinical practice. J Thromb Haemost. 2008; 6:2048-2054.10.1111/j.1538-7836.2008.03187.x18983511Search in Google Scholar

20. MARCUCCI M., MANCUSO M.E., SANTAGOSTINO E., KENET G., ELALFY M., HOLZHAUER S., et al. Type and intensity of FVIII exposure on inhibitor development in PUPs with haemophilia A. A patient-level meta-analysis. Thromb Haemost. 2015; 113:958-967.10.1160/TH14-07-062125631402Search in Google Scholar

21. KURNIK K., BIDLINGMAIER C., ENGL W., CHEHADEH H., REIPERT B., AUERSWALD G. New early prophylaxis regimen that avoids immunological danger signals can reduce FVIII inhibitor development. Haemophilia. 2010; 16:256-262.10.1111/j.1365-2516.2009.02122.x19878331Search in Google Scholar

22. JAMES E.A., VAN HAREN S.D., ETTINGER R.A., FIJNVANDRAAT K., LIBERMAN J.A., KWOK W.W., et al. T-cell responses in two unrelated hemophilia A inhibitor subjects include an epitope at the factor VIII R593C missense site. J Thromb Haemost. 2011; 9:689-699.10.1111/j.1538-7836.2011.04202.x432317821251204Search in Google Scholar

23. YADA K., NOGAMI K., TAKEYAMA M., OGIWARA K., WAKABAYASHI H., SHIMA M. Mild hemophilia A patient with novel Pro1809Leu mutation develops an anti-C2 antibody inhibiting allogeneic but not autologous factor VIII activity. J Thromb Haemost. 2015; 13:1843-1853.10.1111/jth.1311826278069Search in Google Scholar

24. SHIMA M., LILLICRAP D., KRUSE-JARRES R. Alternative therapies for the management of inhibitors. Haemophilia. 2016; 22 Suppl 5:36-41.10.1111/hae.1300527405674Search in Google Scholar

25. LAI J.D., MOOREHEAD P.C., SPONAGLE K., STEINITZ K.N., REIPERT B.M., HOUGH C, et al. Concurrent influenza vaccination reduces anti-FVIII antibody responses in murine hemophilia A. Blood. 2016; 127:3439-3449.10.1182/blood-2015-11-67928227034428Search in Google Scholar

26. LÖVGREN K.M., SØNDERGAARD H., SKOV S., WIINBERG B. Joint bleeds increase the inhibitor response to human factor VIII in a rat model of severe haemophilia A. Haemophilia 2016; 22:772-779.10.1111/hae.1301427439658Search in Google Scholar

27. FISCHER K., LASSILA R., PEYVANDI F., CALIZZANI G., GATT A., LAMBERT T., et al. Inhibitor development in haemophilia according to concentrate. Four-year results from the European HAemophilia Safety Surveillance (EUHASS) project. Thromb Haemost. 2015; 113:968-975.10.1160/TH14-10-082625567324Search in Google Scholar

28. MANCUSO M.E., MANNUCCI P.M., ROCINO A., GARAGIOLA I., TAGLIAFERRI A., SANTAGOSTINO E. Source and purity of factor VIII products as risk factors for inhibitor development in patients with hemophilia A. J Thromb Haemost. 2012; 10:781-790.10.1111/j.1538-7836.2012.04691.x22452823Search in Google Scholar

29. FEISTRITZER C., SCHMIDT S. Reversal of direct oral anticoagulants in hemophilia treatment: ASH meeting 2015. Memo. 2016; 9:131-135.10.1007/s12254-016-0284-2504548327752290Search in Google Scholar

30. MATHEW P., DINTER H., CHURCH N., HUMPHRIES T.J., KULKARNI R. Inhibitors in haemophilia A: a perspective on clotting factor products as a potential contributing factor. Haemophilia. 2016; 22:334-341.10.1111/hae.1288826843214Search in Google Scholar

31. CALVEZ T., CHAMBOST H., CLAEYSSENS-DONADEL S., D’OIRON R., GOULET V., GUILLET B., et al. Recombinant factor VIII products and inhibitor development in previously untreated boys with severe hemophilia A. Blood. 2014; 124:3398-3408.10.1182/blood-2014-07-58634725253771Search in Google Scholar

32. COLLINS P.W., PALMER B.P., CHALMERS E.A., HART D.P., LIESNER R., RANGARAJAN S., 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; 124:3389-3397.10.1182/blood-2014-07-580498424603725339360Search in Google Scholar

33. AZNAR J.A., MORET A., IBÁÑEZ F., VILA C., CABRERA N., MESA E., et al. Inhibitor development after switching of FVIII concentrate in multitransfused patients with severe haemophilia A. Haemophilia. 2014; 20:624-629.10.1111/hae.1243924697977Search in Google Scholar

34. KOCHER S., ASMELASH G., MAKKI V., MÜLLER S., KREKELER S., ALESCI S., et al. Inhibitor development after changing FVIII/IX products in patients with haemophilia. Hamostaseologie. 2012; 32 Suppl 1:S39-42.10.1055/s-0037-1619773Search in Google Scholar

35. PARRA LOPEZ R., NEMES L., JIMENEZ-YUSTE V., RUSEN L., CID A.R., CHARNIGO R.J., et al. Prospective surveillance study of haemophilia A patients switching from moroctocog alfa or other factor VIII products to moroctocog alfa albumin-free cell culture (AF-CC) in usual care settings. Thromb Haemost. 2015; 114:676-684.10.1160/TH14-09-076026293201Search in Google Scholar

36. MANNUCCI P.M., MANCUSO M.E., FRANCHINI M. Tailoring hemostatic therapies to lower inhibitor development in previously untreated patients with severe hemophilia A. J Thromb Haemost. 2016; 14:1330-1336.10.1111/jth.1335627155314Search in Google Scholar

37. KAHLE J., ORLOWSKI A., STICHEL D., HEALEY J.F., PARKER E.T., JAKEMIN M., et al. Frequency and epitope specificity of anti-factor VIII C1 domain antibodies in acquired and congenital hemophilia A. Blood. 2017; pii:blood-2016-11-751347.10.1182/blood-2016-11-751347555357328507083Search in Google Scholar

38. MATINO D., GARGARO M., SANTAGOSTINO E., DI MINNO M.N., CASTAMAN G., MORFINI M., et al. IDO1 suppresses inhibitor development in hemophilia A treated with factor VIII. J Clin Invest. 2015; 125:3766-3781.10.1172/JCI81859460712126426076Search in Google Scholar

39. OLDENBURG J., LACROIX-DESMAZES S., LILLICRAP D. Alloantibodies to therapeutic factor VIII in hemophilia A: the role of von Willebrand factor in regulating factor VIII immunogenicity. Haematologica. 2015; 100:149-156.10.3324/haematol.2014.112821480314725638804Search in Google Scholar

40. MILLER L., WEISSMÜLLER S., RINGLER E., CRAUWELS P., van ZANDBERGEN G., SEITZ R., et al. Danger signal-dependent activation of human dendritic cells by plasma-derived factor VIII products. Thromb Haemost. 2015; 114:268-276.10.1160/TH14-09-078925947149Search in Google Scholar

41. JACQUEMIN M., SAINT-REMY J.M. T cell response to FVIII. Cell Immunol. 2016; 301:8-11.10.1016/j.cellimm.2015.09.00726435345Search in Google Scholar

42. WANG X., SU J., SHERMAN A., ROGERS G.L., LIAO G., HOFFMAN B.E., et al. Plant-based oral tolerance to hemophilia therapy employs a complex immune regulatory response including LAP+CD4+ T cells. Blood. 2015; 125:2418-2427.10.1182/blood-2014-08-597070439201025700434Search in Google Scholar

43. ALLACHER P., BAUMGARTNER C.K., PORDES A.G., AHMAD R.U., SCHWARZ H.P., REIPERT B.M. Stimulation and inhibition of FVIII-specific memory B-cell responses by CpG-B (ODN 1826), a ligand for Toll-like receptor 9. Blood. 2011; 117:259-267.10.1182/blood-2010-06-28900920889922Search in Google Scholar

44. WERWITZKE S., VOLLACK N., VON HORNUNG M., KALIPPKE K., KUTZSCHBACH J., TRUMMER A., et al. Deletion or inhibition of Fc gamma receptor 2B (CD32) prevents FVIII-specific activation of memory B cells in vitro. Thromb Haemost. 2015; 114:1127-1135.10.1160/TH14-06-053526245154Search in Google Scholar

45. BATOROVA A., JANKOVICOVA D., MORONGOVA A., BUBANSKA E., PRIGANCOVA T., HORAKOVA J., et al. Inhibitors in Severe Hemophilia A: 25-Year Experience in Slovakia. Semin Thromb Hemost. 2016; 42:550-562.10.1055/s-0036-158110727235830Search in Google Scholar

46. MANNUCCI P.M., GARAGIOLA I. Factor VIII products in haemophilia A: one size fits all? Thromb Haemost 2015; 113:911-914.10.1160/TH15-04-0273Search in Google Scholar

47. DASGUPTA S., REPESSE Y., BAYRY J., NAVARRETE A.M., WOOTLA B., DELIGNAT S., et al. VWF protects FVIII from endocytosis by dendritic cells and subsequent presentation to immune effectors. Blood. 2007; 109:610–612.10.1182/blood-2006-05-02275616985172Search in Google Scholar

48. QADURA M., WATERS B., BURNETT E., CHEGENI R., BRADSHAW S., HOUGH C., et al. Recombinant and plasma-derived factor VIII products induce distinct splenic cytokine microenvironments in haemophilia A mice. Blood. 2009; 114:871-880.10.1182/blood-2008-09-17464919411636Search in Google Scholar

49. GHIO M., CONTINI P., OTTONELLO L., ARDUINO N., GRINGERI A., INDIVERI F., et al. Effect of clotting factors concentrates on lymphocyte and neutrophil function in vitro. Thromb Haemost. 2003; 89:365–373.10.1055/s-0037-1613454Search in Google Scholar

50. PEYVANDI F., MANNUCCI P.M., GARAGIOLA I., EL-BESHLAWY A., ELALFY M., RAMANAN V., et al. A Randomized Trial of Factor VIII and Neutralizing Antibodies in Hemophilia A. N Engl J Med. 2016; 374:2054-2064.10.1056/NEJMoa151643727223147Search in Google Scholar

51. MANNUCCI P.M., MANCUSO M.E., SANTAGOSTINO E. How we choose factor VIII to treat haemophilia. Blood. 2012; 119:4108-4114.10.1182/blood-2012-01-39441122411872Search in Google Scholar

52. PEYVANDI F., MANNUCCI P.M., PALLA R., ROSENDAAL F.R. SIPPET: methodology, analysis and generalizability. Haemophilia. 2017; 23:353-361.10.1111/hae.1320328306186Search in Google Scholar

53. AFONJA O., KOZAK R., PETRARO P., MICHAELS L.A., MATHEW P., LEMM G., et al. Baby hamster kidney cell-derived recombinant factor VIII: a quarter century of learning and clinical experience. Expert Rev Hematol. 2016; 9:1151-1164.10.1080/17474086.2017.125955927841041Search in Google Scholar

54. HARTMANN J., CROTEAU S.E. 2017 Clinical trials update: Innovations in hemophilia therapy. Am J Hematol. 2016; 91:1252-1260.10.1002/ajh.2454327563744Search in Google Scholar

55. YOON J., SCHMIDT A., ZHANG A.H., KÖNIGS C., KIM Y.C., SCOTT D.W. FVIII-specific human chimeric antigen receptor T-regulatory cells suppress T- and B-cell responses to FVIII. Blood. 2017; 129:238-245.10.1182/blood-2016-07-727834523421928064157Search in Google Scholar

eISSN:
2501-062X
Language:
English
Publication timeframe:
4 times per year
Journal Subjects:
Medicine, Clinical Medicine, Internal Medicine, other, Cardiology, Gastroenterology, Rheumatology