Inhibitors in Patients with Congenital Bleeding Disorders Other Than Hemophilia

Abstract

The most worrying complication of replacement therapy for severe hemophilia A and B is currently the occurrence of inhibitory alloantibodies against infused factor VIII and factor IX, respectively. Inhibitors compromise the management of hemorrhage in affected patients, with a considerable increase in complications, disability, and costs. While these alloantibodies have been extensively studied in the past years in hemophilia A and B, those occurring in patients with other inherited bleeding disorders are less well characterized and still poorly understood, mostly due to the rarity of these hemorrhagic conditions. This narrative review will deal with inhibitors arising in patients with inherited bleeding disorders other than “classical” hemophilia, focusing in particular on those developing in patients with congenital deficiency of coagulation factor V, factor VII, factor XI, and factor XIII.

Keywords

inherited bleeding disorders - alloantibodies - congenital - inhibitors

• References

• 1 Franchini M, Mannucci PM. Hemophilia A in the third millennium. Blood Rev 2013; 27 (04) 179-184
• 2 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; 14 (07) 1330-1336
• 3 Gringeri A, Mantovani LG, Scalone L, Mannucci PM. ; COCIS Study Group. Cost of care and quality of life for patients with hemophilia complicated by inhibitors: the COCIS Study Group. Blood 2003; 102 (07) 2358-2363
• 4 Gringeri A, Mannucci PM. ; Italian Association of Haemophilia Centres. Italian guidelines for the diagnosis and treatment of patients with haemophilia and inhibitors. Haemophilia 2005; 11 (06) 611-619
• 5 Hay CR, Brown S, Collins PW, Keeling DM, Liesner R. The diagnosis and management of factor VIII and IX inhibitors: a guideline from the United Kingdom Haemophilia Centre Doctors Organisation. Br J Haematol 2006; 133 (06) 591-605
• 6 Franchini M, Mannucci PM. Inhibitors of propagation of coagulation (factors VIII, IX and XI): a review of current therapeutic practice. Br J Clin Pharmacol 2011; 72 (04) 553-562
• 7 Astermark J, Santagostino E, Keith Hoots W. Clinical issues in inhibitors. Haemophilia 2010; 16 (Suppl. 05) 54-60
• 8 Franchini M, Coppola A, Tagliaferri A, Lippi G. FEIBA versus NovoSeven in hemophilia patients with inhibitors. Semin Thromb Hemost 2013; 39 (07) 772-778
• 9 Franchini M, Coppola A, Rocino A. , et al; Italian Association of Haemophilia Centers AICE Working Group. Perceived challenges and attitudes to regimen and product selection from Italian haemophilia treaters: the 2013 AICE survey. Haemophilia 2014; 20 (02) e128-e135
• 10 Franchini M, Mannucci PM. Alloantibodies in von Willebrand disease. Semin Thromb Hemost 2018; 44 (06) 590-594
• 11 Poon MC. Alloantibodies in Glanzmann Thrombasthenia and other inherited platelet disorders. Semin Thromb 2018; 44 (06) 604-614
• 12 Lippi G, Favaloro EJ, Montagnana M, Manzato F, Guidi GC, Franchini M. Inherited and acquired factor V deficiency. Blood Coagul Fibrinolysis 2011; 22 (03) 160-166
• 13 Giampaolo A, Vulcano F, Macioce G. , et al. Factor-V expression in platelets from human megakaryocytic culture. Br J Haematol 2005; 128 (01) 108-111
• 14 Asselta R, Peyvandi F. Factor V deficiency. Semin Thromb Hemost 2009; 35 (04) 382-389
• 15 Asselta R, Tenchini ML, Duga S. Inherited defects of coagulation factor V: the hemorrhagic side. J Thromb Haemost 2006; 4 (01) 26-34
• 16 Vos HL. Inherited defects of coagulation factor V: the thrombotic side. J Thromb Haemost 2006; 4 (01) 35-40
• 17 Thalji N, Camire RM. Parahemophilia: new insights into factor v deficiency. Semin Thromb Hemost 2013; 39 (06) 607-612
• 18 Acharya SS, Coughlin A, Dimichele DM. ; North American Rare Bleeding Disorder Study Group. Rare Bleeding Disorder Registry: deficiencies of factors II, V, VII, X, XIII, fibrinogen and dysfibrinogenemias. J Thromb Haemost 2004; 2 (02) 248-256
• 19 Makris M, Calizzani G, Fischer K. , et al. The European Haemophilia Network (EUHANET). Blood Transfus 2014; 12 (Suppl. 03) s515-s518
• 20 Guasch JF, Cannegieter S, Reitsma PH, van't Veer-Korthof ET, Bertina RM. Severe coagulation factor V deficiency caused by a 4 bp deletion in the factor V gene. Br J Haematol 1998; 101 (01) 32-39
• 21 Vos HL. An online database of mutations and polymorphisms in and around the coagulation factor V gene. J Thromb Haemost 2007; 5 (01) 185-188
• 22 Peyvandi F, Bolton-Maggs PH, Batorova A, De Moerloose P. Rare bleeding disorders. Haemophilia 2012; 18 (Suppl. 04) 148-153
• 23 Murray JM, Rand MD, Egan JO, Murphy S, Kim HC, Mann KG. Factor V New Brunswick: Ala221-to-Val substitution results in reduced cofactor activity. Blood 1995; 86 (05) 1820-1827
• 24 Franchini M, Lippi G. Acquired factor V inhibitors: a systematic review. J Thromb Thrombolysis 2011; 31 (04) 449-457
• 25 Lak M, Sharifian R, Peyvandi F, Mannucci PM. Symptoms of inherited factor V deficiency in 35 Iranian patients. Br J Haematol 1998; 103 (04) 1067-1069
• 26 Peyvandi F, Di Michele D, Bolton-Maggs PHB, Lee CA, Tripodi A, Srivastava A. ; Project on Consensus Definitions in Rare Bleeeding Disorders of the Factor VIII/Factor IX Scientific and Standardisation Committee of the International Society on Thrombosis and Haemostasis. Classification of rare bleeding disorders (RBDs) based on the association between coagulant factor activity and clinical bleeding severity. J Thromb Haemost 2012; 10 (09) 1938-1943
• 27 Duckers C, Simioni P, Rosing J, Castoldi E. Advances in understanding the bleeding diathesis in factor V deficiency. Br J Haematol 2009; 146 (01) 17-26
• 28 Di Paola J, Nugent D, Young G. Current therapy for rare factor deficiencies. Haemophilia 2001; 7 (Suppl. 01) 16-22
• 29 Peyvandi F, Duga S, Akhavan S, Mannucci PM. Rare coagulation deficiencies. Haemophilia 2002; 8 (03) 308-321
• 30 Mumford AD, Ackroyd S, Alikhan R. , et al; BCSH Committee. Guideline for the diagnosis and management of the rare coagulation disorders: a United Kingdom Haemophilia Centre Doctors' Organization guideline on behalf of the British Committee for Standards in Haematology. Br J Haematol 2014; 167 (03) 304-326
• 31 Peyvandi F, Menegatti M. Treatment of rare factor deficiencies in 2016. Hematology (Am Soc Hematol Educ Program) 2016; 2016 (01) 663-669
• 32 Peyvandi F, Garagiola I, Biguzzi E. Advances in the treatment of bleeding disorders. J Thromb Haemost 2016; 14 (11) 2095-2106
• 33 Cicchetti A, Berrino A, Casini M. , et al. Health Technology Assessment of pathogen reduction technologies applied to plasma for clinical use. Blood Transfus 2016; 14 (04) 287-386
• 34 Vaglio S, Prisco D, Biancofiore G. , et al. Recommendations for the implementation of a Patient Blood Management programme. Application to elective major orthopaedic surgery in adults. Blood Transfus 2016; 14 (01) 23-65
• 35 Mannucci PM, Peyvandi F, Franchini M. Rare inherited coagulation disorders other than hemophilia. In: White GC, Marder VJ, Aird WC, Bennet JS, Schulman S. , eds. Hemostasis and Thrombosis. Basic Principles and Clinical Practice. Philadelphia, PA: Lippincott Williams and Wilkins; 2013
• 36 Fratantoni JC, Hilgartner M, Nachman RL. Nature of the defect in congenital factor V deficiency: study in a patient with an acquired circulating anticoagulant. Blood 1972; 39 (06) 751-758
• 37 Mazzucconi MG, Solinas S, Chistolini A, Motta M, Mariani G. Inhibitor to factor V in severe factor V congenital deficiency. A case report. Nouv Rev Fr Hematol 1985; 27 (05) 303-305
• 38 Salooja N, Martin P, Khair K, Liesner R, Hann I. Severe factor V deficiency and neonatal intracranial haemorrhage: a case report. Haemophilia 2000; 6 (01) 44-46
• 39 Lee WS, Chong LA, Begum S, Abdullah WA, Koh MT, Lim EJ. Factor V inhibitor in neonatal intracranial hemorrhage secondary to severe congenital factor V deficiency. J Pediatr Hematol Oncol 2001; 23 (04) 244-246
• 40 Divanon F, Hecquard C, Borel-Derlon A. Experience with use of recombinant activated factor VII. J Clin Pharm Ther 2002; 27 (02) 133-138
• 41 Perez Botero J, Burns D, Thompson CA, Pruthi RK. Successful treatment with thalidomide of a patient with congenital factor V deficiency and factor V inhibitor with recurrent gastrointestinal bleeding from small bowel arteriovenous malformations. Haemophilia 2013; 19 (01) e59-e61
• 42 Bolton-Maggs PH, Perry DJ, Chalmers EA. , et al. The rare coagulation disorders--review with guidelines for management from the United Kingdom Haemophilia Centre Doctors' Organisation. Haemophilia 2004; 10 (05) 593-628
• 43 Lollar P. Pathogenic antibodies to coagulation factors. Part II. Fibrinogen, prothrombin, thrombin, factor V, factor XI, factor XII, factor XIII, the protein C system and von Willebrand factor. J Thromb Haemost 2005; 3 (07) 1385-1391
• 44 Ang AL, Kuperan P, Ng CH, Ng HJ. Acquired factor V inhibitor. A problem-based systematic review. Thromb Haemost 2009; 101 (05) 852-859
• 45 Knöbl P, Lechner K. Acquired factor V inhibitors. Baillieres Clin Haematol 1998; 11 (02) 305-318
• 46 Chediak J, Ashenhurst JB, Garlick I, Desser RK. Successful management of bleeding in a patient with factor V inhibitor by platelet transfusions. Blood 1980; 56 (05) 835-841
• 47 Gavva C, Yates SG, Rambally S, Sarode R. Transfusion management of factor V deficiency: three case reports and review of the literature. Transfusion 2016; 56 (07) 1745-1749
• 48 Ragni MV, Lewis JH, Spero JA, Hasiba U. Factor VII deficiency. Am J Hematol 1981; 10 (01) 79-88
• 49 Mariani G, Bernardi F. Factor VII Deficiency. Semin Thromb Hemost 2009; 35 (04) 400-406
• 50 van 't Hooft FM, Silveira A, Tornvall P. , et al. Two common functional polymorphisms in the promoter region of the coagulation factor VII gene determining plasma factor VII activity and mass concentration. Blood 1999; 93 (10) 3432-3441
• 51 Triplett DA, Brandt JT, Batard MA, Dixon JL, Fair DS. Hereditary factor VII deficiency: heterogeneity defined by combined functional and immunochemical analysis. Blood 1985; 66 (06) 1284-1287
• 52 McVey JH, Boswell E, Mumford AD, Kemball-Cook G, Tuddenham EG. Factor VII deficiency and the FVII mutation database. Hum Mutat 2001; 17 (01) 3-17
• 53 Mariani G, Herrmann FH, Dolce A. , et al; International Factor VII Deficiency Study Group. Clinical phenotypes and factor VII genotype in congenital factor VII deficiency. Thromb Haemost 2005; 93 (03) 481-487
• 54 Peyvandi F, Garagiola I, Palla R, Marziliano N, Mannucci PM. Role of the 2 adenine (g.11293_11294insAA) insertion polymorphism in the 3′ untranslated region of the factor VII (FVII) gene: molecular characterization of a patient with severe FVII deficiency. Hum Mutat 2005; 26 (05) 455-461
• 55 Peyvandi F, Jenkins PV, Mannucci PM. , et al. Molecular characterisation and three-dimensional structural analysis of mutations in 21 unrelated families with inherited factor VII deficiency. Thromb Haemost 2000; 84 (02) 250-257
• 56 Giansily-Blaizot M, Aguilar-Martinez P, Biron-Andreani C, Jeanjean P, Igual H, Schved JF. ; Study Group of Factor Seven Deficiency. Analysis of the genotypes and phenotypes of 37 unrelated patients with inherited factor VII deficiency. Eur J Hum Genet 2001; 9 (02) 105-112
• 57 Di Minno MN, Dolce A, Mariani G. ; STER Study Group. Bleeding symptoms at disease presentation and prediction of ensuing bleeding in inherited FVII deficiency. Thromb Haemost 2013; 109 (06) 1051-1059
• 58 Quintavalle G, Riccardi F, Rivolta GF. , et al; Ad-Hoc Study Group. F7 gene variants modulate protein levels in a large cohort of patients with factor VII deficiency. Results from a genotype-phenotype study. Thromb Haemost 2017; 117 (08) 1455-1464
• 59 Herrmann FH, Wulff K, Auerswald G. , et al; Greifswald Factor FVII Deficiency Study Group. Factor VII deficiency: clinical manifestation of 717 subjects from Europe and Latin America with mutations in the factor 7 gene. Haemophilia 2009; 15 (01) 267-280
• 60 Peyvandi F, Mannucci PM, Asti D, Abdoullahi M, DI Rocco N, Sharifian R. Clinical manifestations in 28 Italian and Iranian patients with severe factor VII deficiency. Haemophilia 1997; 3 (04) 242-246
• 61 Marty S, Barro C, Chatelain B. , et al. The paradoxical association between inherited factor VII deficiency and venous thrombosis. Haemophilia 2008; 14 (03) 564-570
• 62 Franchini M, Lippi G. Recombinant activated factor VII: mechanisms of action and current indications. Semin Thromb Hemost 2010; 36 (05) 485-492
• 63 Mariani G, Konkle BA, Ingerslev J. Congenital factor VII deficiency: therapy with recombinant activated factor VII -- a critical appraisal. Haemophilia 2006; 12 (01) 19-27
• 64 Mariani G, Dolce A, Batorova A. , et al; STER and the International Factor VII Deficiency Study Groups. Recombinant, activated factor VII for surgery in factor VII deficiency: a prospective evaluation - the surgical STER. Br J Haematol 2011; 152 (03) 340-346
• 65 Nicolaisen EM, Hansen LL, Poulsen F, Glazer S, Hedner U. Immunological aspects of recombinant factor VIIa (rFVIIa) in clinical use. Thromb Haemost 1996; 76 (02) 200-204
• 66 Ingerslev J, Christiansen K, Sørensen B. ; International Registry on Factor VII Deficiency (IRF7) Steering Committee. Inhibitor to factor VII in severe factor VII deficiency: detection and course of the inhibitory response. J Thromb Haemost 2005; 3 (04) 799-800
• 67 Pruthi RK, Rodriguez V, Allen C, Slaby JA, Schmidt KA, Plumhoff EA. Molecular analysis in a patient with severe factor VII deficiency and an inhibitor: report of a novel mutation (S103G). Eur J Haematol 2007; 79 (04) 354-359
• 68 Tokgoz H, Caliskan U, Lavigne-Lissalde G, Giansily-Blaizot M. Successful prophylactic use of recombinant activated factor VII (rFVIIa) in a patient with congenital FVII deficiency and inhibitors to FVII. Haemophilia 2012; 18 (01) e25-e27
• 69 Mariani G, Napolitano M, Dolce A. , et al; Seven Treatment Evaluation Registry; International Factor VII Deficiency Study Group. Replacement therapy for bleeding episodes in factor VII deficiency. A prospective evaluation. Thromb Haemost 2013; 109 (02) 238-247
• 70 Batorova A, Mariani G, Kavakli K. , et al; STER Study Group. Inhibitors to factor VII in congenital factor VII deficiency. Haemophilia 2014; 20 (02) e188-e191
• 71 Borhany M, Delbes C, Giansily-Blaizot M. , et al. A new report of FVII-inhibitor in a patient suffering from severe congenital FVII deficiency. Haemophilia 2015; 21 (04) e336-e338
• 72 See WS, Chang KO, Cheuk DK. , et al. Inhibitor development after liver transplantation in congenital factor VII deficiency. Haemophilia 2016; 22 (05) e417-e422
• 73 Duga S, Salomon O. Factor XI Deficiency. Semin Thromb Hemost 2009; 35 (04) 416-425
• 74 Franchini M, Veneri D, Lippi G. Inherited factor XI deficiency: a concise review. Hematology 2006; 11 (05) 307-309
• 75 Seligsohn U. Factor XI deficiency in humans. J Thromb Haemost 2009; 7 (Suppl. 01) 84-87
• 76 James P, Salomon O, Mikovic D, Peyvandi F. Rare bleeding disorders - bleeding assessment tools, laboratory aspects and phenotype and therapy of FXI deficiency. Haemophilia 2014; 20 (Suppl. 04) 71-75
• 77 Asakai R, Chung DW, Davie EW, Seligsohn U. Factor XI deficiency in Ashkenazi Jews in Israel. N Engl J Med 1991; 325 (03) 153-158
• 78 Mitchell M, Mountford R, Butler R. , et al. Spectrum of factor XI (F11) mutations in the UK population--116 index cases and 140 mutations. Hum Mutat 2006; 27 (08) 829
• 79 Soldà G, Asselta R, Ghiotto R, Tenchini ML, Castaman G, Duga S. A type II mutation (Glu117stop), induction of allele-specific mRNA degradation and factor XI deficiency. Haematologica 2005; 90 (12) 1716-1718
• 80 Zadra G, Asselta R, Tenchini ML. , et al. Simultaneous genotyping of coagulation factor XI type II and type III mutations by multiplex real-time polymerase chain reaction to determine their prevalence in healthy and factor XI-deficient Italians. Haematologica 2008; 93 (05) 715-721
• 81 Salomon O, Steinberg DM, Seligshon U. Variable bleeding manifestations characterize different types of surgery in patients with severe factor XI deficiency enabling parsimonious use of replacement therapy. Haemophilia 2006; 12 (05) 490-493
• 82 Peyvandi F, Lak M, Mannucci PM. Factor XI deficiency in Iranians: its clinical manifestations in comparison with those of classic hemophilia. Haematologica 2002; 87 (05) 512-514
• 83 Myers B, Pavord S, Kean L, Hill M, Dolan G. Pregnancy outcome in Factor XI deficiency: incidence of miscarriage, antenatal and postnatal haemorrhage in 33 women with Factor XI deficiency. BJOG 2007; 114 (05) 643-646
• 84 Salomon O, Steinberg DM, Tamarin I, Zivelin A, Seligsohn U. Plasma replacement therapy during labor is not mandatory for women with severe factor XI deficiency. Blood Coagul Fibrinolysis 2005; 16 (01) 37-41
• 85 Santagostino E, Mancuso ME, Morfini M. , et al. Solvent/detergent plasma for prevention of bleeding in recessively inherited coagulation disorders: dosing, pharmacokinetics and clinical efficacy. Haematologica 2006; 91 (05) 634-639
• 86 Salomon O, Zivelin A, Livnat T, Seligsohn U. Inhibitors to Factor XI in patients with severe Factor XI deficiency. Semin Hematol 2006; 43 (01) (Suppl. 01) S10-S12
• 87 Zucker M, Zivelin A, Teitel J, Seligsohn U. Induction of an inhibitor antibody to factor XI in a patient with severe inherited factor XI deficiency by Rh immune globulin. Blood 2008; 111 (03) 1306-1308
• 88 Salomon O, Zivelin A, Livnat T. , et al. Prevalence, causes, and characterization of factor XI inhibitors in patients with inherited factor XI deficiency. Blood 2003; 101 (12) 4783-4788
• 89 Hedner U. Factor VIIa in the treatment of haemophilia. Blood Coagul Fibrinolysis 1990; 1 (03) 307-317
• 90 Billon S, Le Niger C, Escoffre-Barbe M, Vicariot M, Abgrall JF. The use of recombinant factor VIIa (NovoSeven) in a patient with a factor XI deficiency and a circulating anticoagulant. Blood Coagul Fibrinolysis 2001; 12 (07) 551-553
• 91 Lawler P, White B, Pye S. , et al. Successful use of recombinant factor VIIa in a patient with inhibitor secondary to severe factor XI deficiency. Haemophilia 2002; 8 (02) 145-148
• 92 Bern MM, Sahud M, Zhukov O, Qu K, Mitchell Jr W. Treatment of factor XI inhibitor using recombinant activated factor VIIa. Haemophilia 2005; 11 (01) 20-25
• 93 Salomon O, Steinberg DM, Dardik R. , et al. Inherited factor XI deficiency confers no protection against acute myocardial infarction. J Thromb Haemost 2003; 1 (04) 658-661
• 94 Livnat T, Zivelin A, Martinowitz U, Salomon O, Seligsohn U. Prerequisites for recombinant factor VIIa-induced thrombin generation in plasmas deficient in factors VIII, IX or XI. J Thromb Haemost 2006; 4 (01) 192-200
• 95 Livnat T, Tamarin I, Mor Y. , et al. Recombinant activated factor VII and tranexamic acid are haemostatically effective during major surgery in factor XI-deficient patients with inhibitor antibodies. Thromb Haemost 2009; 102 (03) 487-492
• 96 Kenet G, Lubetsky A, Luboshitz J. , et al. Lower doses of rFVIIa therapy are safe and effective for surgical interventions in patients with severe FXI deficiency and inhibitors. Haemophilia 2009; 15 (05) 1065-1073
• 97 Teruya J, Styler M. Management of factor XI inhibitor for cardiac intervention: successful treatment with immunosuppressive therapy and plasma exchange. Haemophilia 2000; 6 (03) 158-161
• 98 Levy JH, Greenberg C. Biology of Factor XIII and clinical manifestations of Factor XIII deficiency. Transfusion 2013; 53 (05) 1120-1131
• 99 Dorgalaleh A, Rashidpanah J. Blood coagulation factor XIII and factor XIII deficiency. Blood Rev 2016; 30 (06) 461-475
• 100 Karimi M, Bereczky Z, Cohan N, Muszbek L. Factor XIII Deficiency. Semin Thromb Hemost 2009; 35 (04) 426-438
• 101 Ichinose A. Physiopathology and regulation of factor XIII. Thromb Haemost 2001; 86 (01) 57-65
• 102 Katona E, Haramura G, Kárpáti L, Fachet J, Muszbek L. A simple, quick one-step ELISA assay for the determination of complex plasma factor XIII (A2B2). Thromb Haemost 2000; 83 (02) 268-273
• 103 Ivaskevicius V, Seitz R, Kohler HP. , et al; Study Group. International registry on factor XIII deficiency: a basis formed mostly on European data. Thromb Haemost 2007; 97 (06) 914-921
• 104 Anwar R, Miloszewski KJ. Factor XIII deficiency. Br J Haematol 1999; 107 (03) 468-484
• 105 Lauer P, Metzner HJ, Zettlmeissl G. , et al. Targeted inactivation of the mouse locus encoding coagulation factor XIII-A: hemostatic abnormalities in mutant mice and characterization of the coagulation deficit. Thromb Haemost 2002; 88 (06) 967-974
• 106 Lak M, Peyvandi F, Ali Sharifian A, Karimi K, Mannucci PM. Pattern of symptoms in 93 Iranian patients with severe factor XIII deficiency. J Thromb Haemost 2003; 1 (08) 1852-1853
• 107 Biswas A, Ivaskevicius V, Thomas A, Oldenburg J. Coagulation factor XIII deficiency. Diagnosis, prevalence and management of inherited and acquired forms. Hamostaseologie 2014; 34 (02) 160-166
• 108 Gootenberg JE. Factor concentrates for the treatment of factor XIII deficiency. Curr Opin Hematol 1998; 5 (06) 372-375
• 109 Lovejoy AE, Reynolds TC, Visich JE. , et al. Safety and pharmacokinetics of recombinant factor XIII-A2 administration in patients with congenital factor XIII deficiency. Blood 2006; 108 (01) 57-62
• 110 Muszbek L, Katona É. Diagnosis and management of congenital and acquired FXIII deficiencies. Semin Thromb Hemost 2016; 42 (04) 429-439
• 111 Lassila R. Clinical use of factor XIII concentrates. Semin Thromb Hemost 2016; 42 (04) 440-444
• 112 Carcao M, Fukutake K, Inbal A. , et al. Developing the first recombinant factor XIII for congenital factor XIII deficiency: clinical challenges and successes. Semin Thromb Hemost 2017; 43 (01) 59-68
• 113 Lorand L, Urayama T, De Kiewiet JW, Nossel HL. Diagnostic and genetic studies on fibrin-stabilizing factor with a new assay based on amine incorporation. J Clin Invest 1969; 48 (06) 1054-1064
• 114 Godal HC. An inhibitor to fibrin stabilizing factor (FSF, factor XIII). Scand J Haematol 1970; 7 (01) 43-48
• 115 Godal HC, Ly B. An inhibitor of activated factor XIII, inhibiting fibrin cross-linking but not incorporation of amine into casein. Scand J Haematol 1977; 19 (05) 443-448
• 116 Henriksson P, McDonagh J, Villa M. Type I autoimmune inhibitor of factor XIII in a patient with congenital factor XIII deficiency [abstract]. Thromb Haemost 1983; 50: 272
• 117 Seiving B, Henriksson P, Stenberg P, Nilsson IM. A reversed activity staining procedure for detection of an acquired antibody against factor XIII in a girl with factor XIII deficiency. Br J Haematol 1992; 82 (02) 414-416
• 118 Rivard GE, St Louis J, Lacroix S, Champagne M, Rock G. Immunoadsorption for coagulation factor inhibitors: a retrospective critical appraisal of 10 consecutive cases from a single institution. Haemophilia 2003; 9 (06) 711-716
• 119 Pénzes K, Vezina C, Bereczky Z. , et al. Alloantibody developed in a factor XIII A subunit deficient patient during substitution therapy; characterization of the antibody. Haemophilia 2015; 22: 268-275
• 120 Wada H, Souri M, Matsumoto R, Sugihara T, Ichinose A. Alloantibodies against the B subunit of plasma factor XIII developed in its congenital deficiency. Thromb Haemost 2013; 109 (04) 661-668
• 121 Inbal A, Oldenburg J, Carcao M, Rosholm A, Tehranchi R, Nugent D. Recombinant factor XIII: a safe and novel treatment for congenital factor XIII deficiency. Blood 2012; 119 (22) 5111-5117